One Health: Animal Models of Heritable Human Bleeding Diseases
Abstract
:Simple Summary
Abstract
1. Introduction
2. Inherited Hemostatic Disorders in People and Animals
2.1. Hemophilia A (Factor VIII: C Deficiency)
2.2. Hemophilia B (Factor IX Deficiency; Christmas Disease)
2.3. von Willebrand Disease (vWD)
2.4. Inherited Platelet Function Defects
2.5. Other Inherited Disorders
2.5.1. Factor VII Deficiency
2.5.2. Factor X Deficiency
2.5.3. Factor XI (PTA) Deficiency
2.5.4. Prekallikrein (Fletcher Factor) Deficiency
2.5.5. Factor XII Deficiency (Hageman Trait)
3. Discussion and Conclusions
4. Conclusions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Hotaling, S.; Kelley, J.L.; Frandsen, P.B. Toward a genome sequence for every animal: Where are we now? Proc. Natl. Acad. Sci. USA 2021, 118, e2109019118. [Google Scholar] [CrossRef]
- Alliance for Regenerative Medicine. A new era in the therapeutic journey—Gene therapy as the beacon for rare diseases. In White Paper; Perkin-Elmer Inc.: Waltham, MA, USA, 2021. [Google Scholar]
- Knutsen, A. CRISPR-Based Therapeutics Blaze an In Vivo Path to the Clinic. Genet. Eng. Biotechnol. News 2021, 41, S12, S14–S15. [Google Scholar] [CrossRef]
- Zhang, F. Development of CRISPR-Cas systems for genome editing and beyond. Q. Rev. Biophys. 2019, 52, 31. [Google Scholar] [CrossRef] [Green Version]
- Xu, X.; Chemparathy, A.; Zeng, L.; Kempton, H.R.; Shang, S.; Nakamura, M.; Qi, L.S. Engineered miniature CRISPR-Cas system for mammalian genome regulation and editing. Mol. Cell 2021, 81, 4333–4345. [Google Scholar] [CrossRef] [PubMed]
- Malech, H.L. Treatment by CRISPR-Cas9 gene editing—A proof of principle. N. Engl. J. Med. 2021, 384, 286–287. [Google Scholar] [CrossRef]
- Musunuru, K. CRISPR hits home in a first-in-human study. CRISPR J. 2021, 4, 460. [Google Scholar] [CrossRef]
- Miccio, A. CRISPR’s path to the clinic. CRISPR J. 2022, 5, 2–3. [Google Scholar] [CrossRef] [PubMed]
- Livshits, G. CRISPR genome editing: Into the second decade. GEN Biotechnol. 2022, 1, 37–40. [Google Scholar] [CrossRef]
- Labant, M. The Point of Base Editors: Correcting Point Mutations. Genet. Eng. Biotechnol. News 2021, 41, S17–S19. [Google Scholar] [CrossRef]
- Ledford, H. Beyond CRISPR: A guide to the many other ways to edit a genome. Nature 2016, 536, 137. [Google Scholar] [CrossRef] [PubMed]
- Isaacson, W. The Code Breaker: Jennifer Doudna, Gene Editing, and the Future of the Human Race; Simon & Schuster: New York, NY, USA, 2021. [Google Scholar]
- Lapinaite, A.; Knott, G.J.; Palumbo, C.M.; Lin-Shiao, E.; Richter, M.F.; Zhao, K.T.; Beal, P.A.; Liu, D.R.; Doudna, J.A. DNA capture by a CRISPR-Cas9–guided adenine base editor. Science 2020, 369, 566–571. [Google Scholar] [CrossRef] [PubMed]
- Anzalone, A.V.; Randolph, P.B.; Davis, J.R.; Sousa, A.A.; Koblan, L.W.; Levy, J.M.; Chen, P.J.; Wilson, C.; Newby, G.A.; Raguram, A.; et al. Search-and-replace genome editing without double-strand breaks or donor DNA. Nature 2019, 576, 149–157. [Google Scholar] [CrossRef] [PubMed]
- Uddin, F.; Rudin, C.M.; Sen, T. CRISPR Gene Therapy: Applications, Limitations, and Implications for the Future. Front. Oncol. 2020, 10, 1387. [Google Scholar] [CrossRef] [PubMed]
- Kumar, S.R.; Xie, J.; Hu, S.; Ko, J.; Huang, Q.; Brown, H.C.; Srivastava, A.; Markusic, D.M.; Doering, C.B.; Spencer, H.T.; et al. Coagulation factor IX gene transfer to non-human primates using engineered AAV3 capsid and hepatic optimized expression cassette. Mol. Ther. Methods Clin. Dev. 2021, 23, 98–107. [Google Scholar] [CrossRef]
- Mendell, J.R.; Al-Zaidy, S.A.; Rodino-Klapac, L.R.; Goodspeed, K.; Gray, S.J.; Kay, C.N.; Boye, S.L.; Boye, S.E.; George, L.A. Current clinical applications of in vivo gene therapy with AAVs. Mol. Ther. 2021, 29, 464–488. [Google Scholar] [CrossRef]
- Khimani, A.H.; Thirion, C.; Srivastava, A. AAV Vectors Advance the Frontiers of Gene Therapy. Genet. Eng. Biotechnol. News 2022, 42, 38–40. [Google Scholar] [CrossRef]
- Nguyen, G.N.; Everett, J.K.; Kafle, S.; Roche, A.M.; Raymond, H.E.; Leiby, J.; Wood, C.; Assenmacher, C.-A.; Merricks, E.P.; Long, C.T.; et al. A long-term study of AAV gene therapy in dogs with hemophilia A identifies clonal expansions of transduced liver cells. Nat. Biotechnol. 2021, 39, 47–55. [Google Scholar] [CrossRef]
- Nathwani, A.C.; Tuddenham, E.G.D.; Rangarajan, S.; Rosales, C.; McIntosh, J.; Linch, D.C.; Chowdary, P.; Riddell, A.; Pie, A.J.; Harrington, C.; et al. Adenovirus-associated virus vector-mediated gene transfer in hemophilia B. N. Engl. J. Med. 2011, 365, 2357–2365. [Google Scholar] [CrossRef]
- Rangarajan, S.; Walsh, L.; Lester, W.; Perry, D.; Madan, B.; Laffan, M.; Yu, H.; Vettermann, C.; Pierce, G.F.; Wong, W.Y.; et al. AAV5-Factor VIII gene transfer in severe hemophilia A. N. Engl. J. Med. 2017, 377, 2519–2530. [Google Scholar] [CrossRef]
- Markusic, D.M.; Herzog, R.W.; Aslanidi, G.V.; Hoffman, B.E.; Li, B.; Li, M.; Jayandharan, G.R.; Ling, C.; Zolotukhin, I.; Ma, W.; et al. High-efficiency transduction and correction of murine hemophilia B using AAV2 vectors devoid of multiple surface-exposed tyrosines. Mol. Ther. 2010, 18, 2048–2056. [Google Scholar] [CrossRef]
- Brown, H.C.; Doering, C.B.; Herzog, R.W.; Ling, C.; Markusic, D.M.; Spencer, H.T.; Srivastava, A.; Srivastava, A. Development of a Clinical Candidate AAV3 Vector for Gene Therapy of Hemophilia B. Hum. Gene Ther. 2020, 31, 1114–1123. [Google Scholar] [CrossRef]
- Nathwani, A.C.; Reiss, U.; Tuddenham, E.; Chowdary, P.; McIntosh, J.; Riddell, A.; Pie, J.; Mahlangu, J.N.; Recht, M.; Shen, Y.-M.; et al. Adeno-Associated Mediated Gene Transfer for Hemophilia B:8 Year Follow up and Impact of Removing “Empty Viral Particles” on Safety and Efficacy of Gene Transfer. Blood 2019, 132, 491. [Google Scholar] [CrossRef]
- Nathwani, A.C. Gene therapy for hemophilia. Hematology 2019, 2019, 1–8. [Google Scholar] [CrossRef]
- Lacroix-Desmazes, S.; Voorberg, J.; Lillicrap, D.; Scott, D.W.; Pratt, K.P. Tolerating factor VIII: Recent progress. Front. Immunol. 2020, 10, 2991. [Google Scholar] [CrossRef]
- Batty, P.; Lillicrap, D. Hemophilia gene therapy: Approaching the first licensed product. HemaSphere 2021, 5, e540. [Google Scholar] [CrossRef]
- HEMLIBRA® [emicizumab-kxwh] Manufactured. Genentech, Inc. A Member of the Roche Group 1 DNA Way South San Francisco, CA 94080-499. Available online: https://www.hemlibra.com/ (accessed on 5 March 2021).
- Connelly, S.; Mount, J.; Mauser, A.; Gardner, J.; Kaleko, M.; McClelland, A.; Lothrop, C.J. Complete short-term correction of canine hemophilia A by in vivo gene therapy. Blood 1996, 88, 3846–3853. [Google Scholar] [CrossRef] [Green Version]
- U.S. Food and Drug Administration. FDA Approves Emicizumab·Kxwh for Prevention and Reduction of Bleeding in Patients with Hemophilia A with Factor VIII Inhibitors. Hemophilia·Factor viii. Available online: www.fda.gov/drresources-information-approved-drugs/fda-approves-emicizumckxwh-prevention-and-reduction-bleeding-patlents (accessed on 2 October 2022).
- Chowdary, P.; Shapiro, S.; Makris, M.; Evans, G.; Boyce, S.; Talks, K.; Dolan, G.; Reiss, U.; Phillips, M.; Riddell, A.; et al. Phase 1–2 trial of AAVS3 gene therapy in patients with hemophilia B. N. Engl. J. Med. 2022, 387, 237–247. [Google Scholar] [CrossRef]
- Murphy, S.L.; High, K.A. Gene therapy for haemophilia. Br. J. Haematol. 2008, 140, 479–487. [Google Scholar] [CrossRef] [Green Version]
- George, L.A.; Monahan, P.E.; Eyster, M.E.; Sullivan, S.K.; Ragni, M.V.; Croteau, S.E.; Rasko, J.E.; Recht, M.; Samelson-Jones, B.J.; MacDougall, A.; et al. Multiyear Factor VIII Expression after AAV Gene Transfer for Hemophilia A. N. Engl. J. Med. 2021, 385, 1961–1973. [Google Scholar] [CrossRef]
- Lawrence, L. Gene Therapy and the Future of Hemophilia Treatment. AABB News. 6–10 September 2022. Available online: www.aabb.org (accessed on 2 October 2022).
- Wachter, K. Biotherapy trials transform care for patients with blood disorders. AABB News 2022, 24, 16–20. [Google Scholar]
- Dodds, W.J. Estimating disease prevalence by health surveys and genetic screening. Adv. Vet. Sci. Comp. Med. 1995, 39, 29–96. [Google Scholar] [PubMed]
- Dodds, W.J. Hemostasis. In Clinical Biochemistry of Domestic Animals, 5th ed.; Kaneko, J.J., Bruss, D., Eds.; Academic Press: San Diego, CA, USA, 1997; pp. 1241–1283. [Google Scholar]
- Owen, C.A., Jr. A History of Blood Coagulation; Nichols, W.L., Walter Bowie, E.J., Eds.; Mayo Foundation for Medical Education and Research; Mayo Clinic: Rochester, MN, USA, 2001. [Google Scholar]
- Dodds, W.J. Keynote address: Extending frontiers in the art of medicine. In Proceedings of the Milestones in AHVMA, 30th anniversary, AHVMA Meeting, Birmingham, AL, USA, 8–11 September 2012. [Google Scholar]
- Peterson, J.L.; Couto, C.G.; Wellman, M.L. Hemostatic disorders in cats: A retrospective study and review of the literature. J. Vet. Int. Med. 1995, 9, 298–303. [Google Scholar] [CrossRef] [PubMed]
- Stokol, T.; Parry, B.W.; Mansell, P.D.; Richardson, J.L. Hematorrhachis associated with hemophilia A in three German shepherd dogs. J. Am. Anim. Hosp. Assoc. 1994, 30, 239–243. [Google Scholar]
- Joseph, S.A.; Brooks, M.B.; Coccari, P.J.; Riback, S.C. Hemophilia A in a German shorthaired pointer: Clinical presentations and diagnosis. J. Am. Anim. Hosp. Assoc. 1995, 32, 25–28. [Google Scholar] [CrossRef] [PubMed]
- Brinkhous, K.M.; Davis, P.D.; Graham, J.B.; Dodds, W.J. Expression and linkage of genes for X-linked hemophilias A and B in the dog. Blood 1973, 41, 577–585. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Feldman, D.G.; Brooks, M.B.; Dodds, W.J. Hemophilia B (factor IX deficiency) in a family of German shepherd dogs. J. Am. Vet. Med. Assoc. 1995, 206, 1901–1905. [Google Scholar]
- Maggio-Price, L.; Dodds, W.J. Factor IX deficiency (hemophilia B) in a family of British shorthair cats. J. Am. Vet. Med. Assoc. 1993, 203, 1702–1704. [Google Scholar]
- Dodds, W.J.; Moynihan, A.C.; Fisher, T.M.; Trauner, D.B. The frequencies of inherited blood and eye diseases as determined by genetic screening programs. J. Am. Anim. Hosp. Assoc. 1981, 17, 697–704. [Google Scholar]
- Dodds, W.J. Contributions and future directions of hemostasis research. J. Am. Vet. Med. Assoc. 1988, 193, 1157–1160. [Google Scholar] [PubMed]
- Stefanon, G.; Stefanon, B.; Stefanon, G.G.; Dodds, W.J. Inherited and acquired canine bleeding disorders in northeastern Italy. Canine Pract. 1993, 18, 15–23. [Google Scholar]
- Brooks, M. Hereditary bleeding disorders in dogs and cats. Vet. Med. 1999, 94, 555–564. [Google Scholar]
- Powell, J.S. Recombinant factor VIII in the management of hemophilia A: Current use and future promise. Ther. Clin. Risk. Manag. 2009, 5, 391–402. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lozier, J.N.; Nichols, T.C. Animal models of hemophilia and related bleeding disorders. Semin. Hematol. 2013, 50, 175–184. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Young, G.; Mahlangu, J.; Kulkarni, R.; Nolan, B.; Liesner, R.; Pasi, J.; Barnes, C.; Neelakantan, S.; Gambino, G.; Cristiano, L.M.; et al. Recombinant factor VIII Fc fusion protein for the prevention and treatment of bleeding in children with severe hemophilia A. Thromb. Haemost. 2015, 13, 967–977. [Google Scholar] [CrossRef] [PubMed]
- Brinkhous, K.M. Gene transfer in the hemophilias: Retrospect and prospect. Thromb. Res. 1992, 67, 329–338. [Google Scholar] [CrossRef] [PubMed]
- Bouma, B.N.; Dodds, W.J.; van Mourik, J.A.; Sixma, J.J.; Webster, W.P. Infusion of human and canine factor VIII in dogs with von Willebrand’s disease: Studies of the von Willebrand and factor VIII synthesis stimulating factors. Scand. J. Haematol. 1976, 17, 263–275. [Google Scholar] [CrossRef] [PubMed]
- Giles, A.R.; Tinlin, S.; Hoogendoorn, H.; Fournel, M.A.; Ng, P.; Pancham, N. In vivo characterization of recombinant factor VIII in a canine model of hemophilia A (factor VIII deficiency). Blood 1988, 72, 335–339. [Google Scholar] [CrossRef]
- Christopherson, P.W.; Bacek, L.M.; King, K.B.; Boudreaux, M.K. Two novel missense mutations associated with hemophilia A in a family of Boxers, and a German Shepherd dog. Vet. Clin. Pathol. 2014, 43, 312–316. [Google Scholar] [CrossRef]
- Brinkhous, K.; Sigman, J.; Read, M.; Stewart, P.; McCarthy, K.; Timony, G.; Leppanen, S.; Rup, B.; Keith, J.J.; Garzone, P.; et al. Recombinant human factor IX: Replacement therapy, prophylaxis, and pharmacokinetics in canine hemophilia B. Blood 1986, 88, 2603–2610. [Google Scholar] [CrossRef] [Green Version]
- Evans, J.P.; Brinkhous, K.M.; Brayer, G.D.; Reisner, H.M.; High, K.A. Canine hemophilia B resulting from a point mutation with unusual consequences. Proc. Natl. Acad. Sci. USA 1989, 86, 10095–10099. [Google Scholar] [CrossRef] [Green Version]
- Mount, J.D.; Herzog, R.W.; Tillson, D.M.; Goodman, S.A.; Robinson, N.; McCleland, M.L.; Bellinger, D.; Nichols, T.C.; Arruda, V.R.; Lothrop, C.D.; et al. Sustained phenotypic correction of hemophilia B dogs with a factor IX null mutation by liver-directed gene therapy. Blood 2002, 99, 2670–2676. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Brooks, M.B.; Gu, W.; Barnas, J.L.; Ray, J.; Ray, K. A Line 1 insertion in the factor IX gene segregates with mild hemophilia B in dogs. Mamm. Genome 2003, 14, 788–795. [Google Scholar] [CrossRef] [PubMed]
- Margaritis, P.; Roy, E.; Aljamali, M.N.; Downey, H.D.; Giger, U.; Zhou, S.; Merricks, E.; Dillow, A.; Ezban, M.; Nichols, T.C.; et al. Successful treatment of canine hemophilia by continuous expression of canine FVIIa. Blood 2009, 113, 3682–3689. [Google Scholar] [CrossRef] [PubMed]
- Margaritis, P. Long-term expression of canine FVIIa in hemophilic dogs. Thromb. Res. 2010, 125 (Suppl. 1), S60–S62. [Google Scholar] [CrossRef] [Green Version]
- Brenig, B.; Steingräber, L.; Shan, S.; Xu, F.; Hirschfeld, M.; Andag, R.; Spengeler, M.; Dietschi, E.; Mischke, R.; Leeb, T. Christmas disease in a Hovawart family resembling human hemophilia B Leyden is caused by a single nucleotide deletion in a highly conserved transcription factor binding site of the F9 gene promoter. Haematologica 2019, 104, 2307–2313. [Google Scholar] [CrossRef] [Green Version]
- Dodds, W.J. Canine von Willebrand’s disease. J. Lab. Clin. Med. 1970, 76, 713–721. [Google Scholar]
- Dodds, W.J. Further studies of canine von Willebrand’s disease. Blood 1975, 45, 221–230. [Google Scholar] [CrossRef] [Green Version]
- Brinkhous, K.M.; Sandberg, H.; Garris, J.B.; Mattsson, C.; Palm, M.; Griggs, T.; Read, M.S. Purified human factor VIII procoagulant protein: Comparative hemostatic response after infusions into hemophilic and von Willebrand disease dogs. Proc. Natl. Acad. Sci. USA 1985, 82, 8752–8756. [Google Scholar] [CrossRef]
- Brinkhous, K.M.; Hedner, U.; Garris, J.B.; Diness, V.; Read, M.S. Effect of recombinant factor VIIa on the hemostatic defect in dogs with hemophilia A, hemophilia B, and von Willebrand disease. Proc. Natl. Acad. Sci. USA 1989, 86, 1382–1386. [Google Scholar] [CrossRef] [Green Version]
- Raymond, S.L.; Jones, D.W.; Brooks, M.B.; Dodds, W.J. Clinical and laboratory features of a severe form of von Willebrand disease in Shetland sheepdogs. J. Am. Vet. Med. Assoc. 1990, 197, 1342–1346. [Google Scholar]
- Meyers, K.; Wardrop, K.; Dodds, W.; Brassard, J. Effect of exercise, DDAVP, and epinephrine on the factor VIII:C-von Willebrand factor complex in normal dogs and von Willebrand factor deficient Doberman pinscher dogs. Thromb. Res. 1990, 57, 97–108. [Google Scholar] [CrossRef] [PubMed]
- Brooks, M.; Leith, G.S.; Allen, A.K.; Woods, P.R.; Benson, R.E.; Dodds, W.J. Bleeding disorder (von Willebrand disease) in a quarter horse. J. Am. Vet. Med. Assoc. 1991, 198, 114–116. [Google Scholar] [PubMed]
- Brooks, M.; Dodds, W.J.; Raymond, S.L. Epidemiologic features of von Willebrand’s disease in Doberman Pinchers, Scottish Terriers, and Shetland Sheepdogs: 260 cases (1984-1988). J. Am. Vet. Med. Assoc. 1992, 200, 1123–1127. [Google Scholar] [PubMed]
- Dodds, W.J. Hypothyroidism and von Willebrand factor. J. Am. Vet. Med. Assoc. 1995, 206, 594–595. [Google Scholar]
- Brooks, M.B.; Raymond, S.L.; Catalfamo, J.L. A severe recessive form of von Willebrand’s disease in German Wirehaired Pointers. J, Am. Vet. Med. Assoc. 1996, 209, 926–929. [Google Scholar]
- Brooks, M.; Raymond, S.; Catalfamo, J. Plasma von Willebrand factor antigen concentration as a predictor of von Willebrand’s disease status in German Wirehaired Pointers. J. Am. Vet. Med. Assoc. 1996, 209, 930–933. [Google Scholar]
- Turecek, P.L.; Gritsch, H.; Pichler, L.; Auer, W.; Fischer, B.; Mitterer, A.; Mundt, W.; Schlokat, U.; Dorner, F.; Brinkman, H.J.M.; et al. In vivo characterization of recombinant von Willebrand factor in dogs with von Willebrand disease. Blood 1997, 90, 3555–3567. [Google Scholar] [CrossRef]
- Venta, P.J.; Li, J.; Yuzbasiyan-Gurkan, V.; Brewer, G.J.; Schall, W.D. Mutation causing von Willebrand’s disease in Scottish Terriers. J. Vet. Intern. Med. 2000, 14, 10–19. [Google Scholar] [CrossRef]
- Riehl, J.; Okura, M.; Mignot, E.; Nishino, S. Inheritance of von Willebrand’s disease in a colony of Doberman Pinchers. Am. J. Vet. Res. 2000, 61, 115–120. [Google Scholar] [CrossRef] [Green Version]
- Brooks, M.B.; Erb, H.N.; Foureman, P.A.; Ray, K. von Willebrand disease phenotype and von Willebrand marker genotype in Doberman Pinchers. Am. J. Vet. Res. 2001, 62, 364–369. [Google Scholar] [CrossRef]
- van Dongen, A.M.; van Leeuwen, M.; Slappendel, R.J. Canine von Willebrand’s disease type 2 in German wirehair pointers in the Netherlands. Vet. Record 2001, 148, 80–82. [Google Scholar] [CrossRef] [PubMed]
- Brooks, M.; Castillo-Juárez, H.; Oltenacu, P. Heritability of plasma von Willebrand factor antigen concentration in German Wirehaired pointers. Vet. Q. 2001, 23, 126–128. [Google Scholar] [CrossRef] [PubMed]
- Gadisseur, A.; Berneman, Z.; Schroyens, W.; Michiels, J.J. Laboratory diagnosis of von Willebrand disease type 1/2E (2A subtype IIE), type 1 Vicenza and mild type 1 caused by mutations in the D3, D4, B1-B3 and C1-C2 domains of the von Willebrand factor gene. Role of von Willebrand factor multimers and the von Willebrand factor propeptide/antigen ratio. Acta Haematol. 2009, 121, 128–138. [Google Scholar] [CrossRef] [PubMed]
- Vos-Loohuis, M.; van Oost, B.A.; Dangel, C.; Langbein-Detsch, I.; Leegwater, P.A. A novel VWF variant associated with type 2 von Willebrand disease in German Wirehaired Pointers and German Shorthaired Pointers. Anim. Genet. 2017, 48, 493–496. [Google Scholar] [CrossRef]
- Segert, J.H.; Seidel, J.-M.; Wurzer, W.J.; Geretschlaeger, A.M. vWDI is inherited in an autosomal dominant manner with incomplete penetrance, in the Kromfohrländer breed. Canine Genet. Epidemiol. 2019, 6, 3. [Google Scholar] [CrossRef]
- Donner, J.; Anderson, H.; Davison, S.; Hughes, A.M.; Bouirmane, J.; Lindqvist, J.; Lytle, K.M.; Ganesan, B.; Ottka, C.; Ruotanen, P.; et al. Frequency and distribution of 152 genetic disease variants in over 100,000 mixed breed and purebred dogs. PLoS Genet. 2018, 14, e1007361. [Google Scholar] [CrossRef]
- Hall, C.A.; London, A.R.; Moynihan, A.C.; Dodds, W.J. Hereditary factors VII and IX deficiency in a large kindred. Brit. J. Haematol. 1975, 29, 319–328. [Google Scholar] [CrossRef]
- Dodds, W.J.; Moynihan, A.C.; Benson, R.E.; Hall, C.A. The value of age and sex-matched controls for coagulation studies. Brit. J. Haematol. 1975, 29, 305–317. [Google Scholar] [CrossRef]
- Benson, R.E.; Dodds, W.J. lmmunological characterization of canine factor VIII. Blood 1976, 48, 521–529. [Google Scholar] [CrossRef] [Green Version]
- Nichols, T.C.; Hough, C.; Agersø, H.; Ezban, M.; Lillicrap, D. Canine models of inherited bleeding disorders in the development of coagulation assays, novel protein replacement and gene therapies. J. Thromb. Haemost. 2016, 14, 894–905. [Google Scholar] [CrossRef] [Green Version]
- Callan, M.B.; Aljamali, M.N.; Margaritis, P.; Griot-Wenk, M.E.; Pollak, E.S.; Werner, P.; Giger, U.; High, K.A. A novel missense mutation responsible for factor VII deficiency in research Beagle colonies. J. Thromb. Haemost. 2006, 4, 2616–2622. [Google Scholar] [CrossRef]
- Dodds, W.J. Canine factor X (Stuart-Prower factor) deficiency. J. Lab. Clin. Med. 1973, 82, 560–566. [Google Scholar]
- Heuss, J.; Weatherton, L. A case of factor X deficiency in a Chihuahua dog. Can. Vet. J. 2016, 57, 865–868. [Google Scholar] [PubMed]
- Dodds, W.J.; Kull, J.E. Canine factor XI (PTA) deficiency. J. Lab. Clin. Med. 1971, 78, 746–752. [Google Scholar] [PubMed]
- Gentry, P.A.; Ross, M.L. Coagulation factor XI deficiency in Holstein cattle: Expression and distribution of factor XI activity. Can. J. Vet. Res. 1993, 57, 242–247. [Google Scholar]
- Knowler, C.; Giger, U.; Dodds, W.J.; Brooks, M. Factor XI deficiency in Kerry Blue Terriers. J. Am. Vet. Med. Assoc. 1994, 205, 1557–1561. [Google Scholar] [PubMed]
- Tcherneva, E.; Giger, U. Molecular base of coagulation factor XI deficiency in Kerry Blue Terrier. Bulg. J. Vet. Med. 2007, 10, 247–255. [Google Scholar]
- Bender, D.E.; Kloos, M.T.; Pontius, J.U.; Hinsdale, M.E.; Bellinger, D.A. Molecular characterization of cat factor XII gene and identification of a mutation causing factor XII deficiency in a domestic shorthair cat colony. Vet. Pathol. 2015, 52, 312–320. [Google Scholar] [CrossRef] [Green Version]
- Maruyama, H.; Hosoe, H.; Nagamatsu, K.; Kano, R.; Kamata, H. A novel missense mutation in the factor XII gene in a litter of cats with factor XII deficiency. J. Vet. Med. Sci. 2017, 79, 822–826. [Google Scholar] [CrossRef] [Green Version]
- Geor, R.; Jackson, M.L.; Lewis, K.D.; Fretz, P.B. Prekallikrein deficiency in a family of Belgian horses. J. Am. Vet. Med. Assoc. 1990, 197, 741–745. [Google Scholar]
- Okawa, T.; Yanase, T.; Miyama, T.S.; Hiraoka, H.; Baba, K.; Tani, K.; Okuda, M.; Mizuno, T. Prekallikrein deficiency in a dog. J. Vet. Med. Sci. 2011, 73, 107–111. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Otto, C.M.; Dodds, W.J.; Greene, C.E. Factor XII and partial prekallikrein deficiencies in a dog with recurrent gastrointestinal hemorrhage. J. Am. Vet. Med. Assoc. 1991, 198, 129–131. [Google Scholar] [PubMed]
- Dodds, W.J. Familial canine thrombocytopathy. Thromb. Diath. Haemorrh. 1967, 26, 241–248. [Google Scholar]
- Smith, T.P.; Dodds, W.J.; Tartaglia, A.P. Thrombasthenic-thrombopathic thrombocytopenia with giant “Swiss-cheese” platelets: A case report. Ann. Intern. Med. 1973, 79, 828–834. [Google Scholar] [CrossRef]
- Raymond, S.L.; Dodds, W.J. Characterization of the fawn-hooded rat as a model for hemostatic studies. Thromb. Diath. Haemorrh. 1975, 33, 361–369. [Google Scholar] [CrossRef]
- Callan, M.B.; Bennett, J.S.; Phillips, D.K.; E Haskins, M.; E Hayden, J.; Anderson, J.G.; Giger, U. Inherited platelet delta-storage pool disease in dogs causing severe bleeding—An animal model for a specific ADP deficiency. Thromb. Haemost. 1995, 74, 949–953. [Google Scholar] [CrossRef]
- Raymond, S.L.; Dodds, W.J. Platelet membrane glycoproteins in normal dogs and dogs with hemostatic defects. J. Lab. Clin. Med. 1979, 93, 607–613. [Google Scholar]
- Catalfamo, J.; Raymond, S.L.; White, J.G.; Dodds, W.J. Defective platelet-fibrinogen interaction in hereditary canine thrombopathia. Blood 1986, 67, 1568–1577. [Google Scholar] [CrossRef] [PubMed]
- Boudreaux, M.K.; Dodds, W.J.; Slauson, D.O.; Catalfamo, J.L. Evidence for regulatory control of canine platelet phosphodiesterase. Biochem. Blophys.Res. Comm. 1986, 140, 589–594. [Google Scholar] [CrossRef]
- Catalfamo, J.L.; Dodds, W.J. Hereditary and acquired thrombopathias. Vet. Clin. North Am. Small An. Pract. 1988, 18, 185–193. [Google Scholar] [CrossRef]
- Patterson, W.R.; Estry, D.W.; Schwartz, K.A.; Borchert, R.D.; Bell, T.G. Absent platelet aggregation with normal fibrinogen binding in Basset hound hereditary thrombopathy. Thromb. Haemost. 1989, 62, 1011–1015. [Google Scholar] [CrossRef] [PubMed]
- Brooks, M.; Catalfamo, J. Buccal mucosa bleeding time is prolonged in canine models of primary hemostatic disorders. Thromb. Haemost. 1993, 70, 777–780. [Google Scholar] [CrossRef] [PubMed]
- Boudreaux, M.K.; Crager, C.; Dillon, A.; Stanz, K.; Toivio-Kinnucan, M. Identification of an intrinsic platelet function defect in Spitz dogs. J. Vet. Intern. Med. 1994, 8, 93–98. [Google Scholar] [CrossRef] [PubMed]
- Searcy, G.P.; Frojmovic, M.M.; McNicol, A.; Robertson, C.; Wong, T.; Gerrard, J.M. Platelets from bleeding Simmental cattle mobilize calcium, phosphorylate myosin light chain and bind normal numbers of fibrinogen molecules but have abnormal cytoskeletal assembly and aggregation in response to ADP. Thromb. Haemost. 1994, 71, 240–246. [Google Scholar] [PubMed]
- Lipscomb, D.L.; Bourne, C.; Boudreaux, M.K. Two genetic defects in αIIb are associated with type I Glanzmann’s thrombasthenia in a Great Pyrenees dog: A 14-base insertion in Exon 13 and a splicing defect of intron 13. Vet. Pathol. 2000, 37, 581–588. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Boudreaux, M.K.; Catalfamo, J.L. Molecular and genetic basis for thrombasthenic thrombopathia in Otterhounds. Am. J. Vet. Res. 2001, 62, 1797–1804. [Google Scholar] [CrossRef]
- Boudreaux, M.K.; Catalfamo, J.L.; Klok, M. Calcium-diacylglycerol guanine nucleotide exchange factor I gene mutations associated with loss of function in canine platelets. Transl. Res. 2007, 150, 81–92. [Google Scholar] [CrossRef] [Green Version]
- Boudreaux, M.K. Characteristics, diagnosis, and treatment of inherited platelet disorders in mammals. J. Am. Vet. Med. Assoc. 2008, 233, 1251–1259. [Google Scholar] [CrossRef]
- Brooks, M.; Etter, K.; Catalfamo, J.; Brisbin, A.; Bustamante, C.; Merzey, J. A genome-wide linkage scan in German shepherd dogs localizes platelet procoagulant efficiency (scott syndrome) to canine chromosome 27. Gene 2010, 450, 70–75. [Google Scholar] [CrossRef] [Green Version]
- Boudreaux, M.K.; Martin, M. P2Y12 receptor gene mutation associated with postoperative hemorrhage in a Greater Swiss Mountain dog. Vet. Clin. Pathol. 2011, 40, 202–206. [Google Scholar] [CrossRef]
- Dodds, W.J.; Laverdure, D.R. The Canine Thyroid Epidemic; DogWise Publ.: Wenatchee, WA, USA, 2011; 192p. [Google Scholar]
- Marta, G.N.; de Campos, F.P.F. Immune thrombocytopenia and autoimmune thyroid disease: A Controversial Overlap. Autops. Case Rep. 2015, 5, 45–48. [Google Scholar] [CrossRef] [PubMed]
- Lentaigne, C.; Freson, K.; Laffan, M.A.; Turro, E.; Ouwehand, W.H. Inherited platelet disorders: Towards DNA-based diagnosis. Blood 2016, 127, 2814–2823. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Flores, R.S.; Boudreaux, M.K.; Vasquez, B.; Bristow, P.; Aronson, L.R.; Santoro-Beer, K.; Callan, M.B. Heterozygosity for P2Y12 receptor gene mutation associated with postoperative hemorrhage in a Greater Swiss Mountain dog. Vet. Clin. Pathol. 2017, 46, 569–574. [Google Scholar] [CrossRef] [PubMed]
- Gentilini, F.; Turba, M.E.; Giancola, F.; Chiocchetti, R.; Bernardini, C.; Dajbychova, M.; Jagannathan, V.; Drögemüller, M.; Drögemüller, C. A large deletion in the GP9 gene in Cocker Spaniel dogs with Bernard-Soulier syndrome. PLoS ONE 2019, 14, e0220625. [Google Scholar] [CrossRef] [PubMed]
- Cortese, L.; Christopherson, P.W.; Pelagalli, A. Platelet function and therapeutic applications in dogs: Current status and future prospects. Animals 2020, 10, 201. [Google Scholar] [CrossRef]
- Ero, M.; Ng, C.; Sambar, C.; Kain, J. This, that, or both: Platelet aggregation and platelet genetics. Med. Lab. Observ. 2022, 54, 32–34. [Google Scholar]
Species | Date Sequence Published |
---|---|
Human | 2001 |
Mouse | 2002 |
Rat | 2004 |
Chicken | 2004 |
Non-Human Primate | |
Chimpanzee | 2005 |
Rhesus macaque | 2007 |
Orangutan | 2011 |
Dog | 2005 |
Cat | 2007 |
Cow | 2009 |
Horse | 2009 |
Turkey | 2010 |
Pig | 2012 |
Goat | 2017 |
Time Period | Discoveries |
---|---|
1700s | Long after Hippocrates, Aristotle, Celsus and Galen found freshly drawn blood to clot, blood clotting became linked to hemostasis (the cessation of bleeding). |
1800s | Thrombosis first recognized by Virchow; platelets are discovered by Bizzozero; familial bleeding tendency in males (hemophilia) is first recognized. |
1900s | Morawitz described the classical theory of blood coagulation. |
1930–1940s | Disputes arose between scientists about factors that form and dissolve clots; more clotting factor disorders are recognized in people (von Willebrand Disease) and dogs (hemophilia). |
1950s | von Willebrand disease identified in Poland-China pigs; factor VII identified in dog plasma after coumarin therapy prolonged the blood clotting in vitro. |
1970–1980s | von Willebrand Disease described in German Shepherd Dogs imported to North America from Germany, and then in many dog breeds, cats, and rabbits; hemophilia described in cats and horses; factors I, IX, X, XI and XII deficiencies documented in dogs, cats, cattle, goats; and platelet defects described in dogs, rats, and mice. |
1990s–today | More of these bleeding disorders found in domestic and companion animals, including the documentation of familial pre-kallikrein and kallikrein deficiencies. |
Bleeding Disorder | GWAS; Genes | Breeds Affected | References |
---|---|---|---|
Hemophilia A (Factor VIII Deficiency) | Boxer, single nucleotide change C to G at nucleotide 1412 (1412 C>G)in Exon 10, results in arginine to proline at amino acid 471 (P471R) in A2 domain German Shepherd Dog, single nucleotide change G to A at nucleotide 1643 (1643 G>A)in Exon 11, results in tyrosine to cysteine at amino acid 548 (C548Y) in A2 domain | Many, also mixed breeds, cats, horses | [19,21,29,39,43,56] |
Hemophilia B (Christmas Disease; Factor IX Deficiency) | Missense mutation G to nucleotide 1477, glycine 379-glutamic acid Insertional mutation in line 1 of canine FIX gene Nucleoside deletion of transcription factor binding site of FIX gene promotor | Cairn Terrier, Hovawart, German Wired-Haired Pointer (Drathaar), 23 other breeds, and cats | [16,20,33,58,59,60,61,62,63] |
von Willebrand Disease, Types 1, 2, 3 | Type 1, Doberman, homozygous 157-base-pair intragenic marker allele+ heterozygous 1 of 4 extragenic marker alleles Type 2, GSHP nucleotide variant at Exon 28 Type 3, single nucleotide deletion in Exon coding VWF prepeptide (Scottish Terrier), splice site mutation Intron 16 (Dutch Kooiker)VWFc.4937A>G A/A, G/G | Many, prevalent in Doberman Pinscher, Shetland Sheepdog, Scottish Terrier, Golden Retriever, Pembroke Welsh Corgi, Chesapeake Bay Retriever, German Short-Haired Pointer (GSHP), German Wire-Haired Pointer (Drathaar), ~ 50 other breeds, cats, Poland. China swine | [76,77,78,81,82,83,84,88] |
Factor VII Deficiency | Missense G96E mutation at Exon 5. Glycine 26 to Glutamic acid, 31% frequency in breed | Beagle, more than 14 other breeds | [89] |
Factor X Deficiency (Stuart–Prower Disease) | Homozygous deletion of factor X gene(s) is lethal | American Cocker Spaniel, Jack Russell Terrier | [91] |
Factor XI Deficiency | Kerry Blue, mutation of F11 gene, homozygotes affected, 90 bp insertion, Chr16:44477343-44477344, 10 bp duplication (dup GCACAAAGCT) Chr:44477344-44477353 | English Springer Spaniel, Kerry Blue Terrier, and Holstein cattle | [95] |
Factor XII Deficiency (Hageman Trait) | Cats, novel mutation (c.1631 G >C) at Exon 13 of feline F12 gene, results in amino acid change (p.GS54A) | Miniature Poodle, cats, reptiles, marine mammals, birds | [96,97] |
Prekallikrein Deficiency | G to A transversion at Exon 8 | Shih Tzu. American Hairless Terrier, others, and Belgian horse | [99] |
Thrombasthenia (Glanzmann’s Disease); Bernard-Soulier Syndrome | Otterhounds, single nucleotide change at G1193 (1000) at Exon 12 of gene encoding for glycoprotein GPIIb, substitution of histidine for aspartic acid at 398 (367) of calcium -binding domain of GPIIb Single ITGA2B gene mutation on chromosome 9, chr9:19054488-19054488: G>C American Cockers, single glycoprotein 9 (GP9) deletion at Exon coding on chromosome 20 Great Pyrenees, 14-base insertion in Exon 13 and a splicing defect of Intron 13 Deletion of P2Y12 in Greater Swiss Mountain Dog and Bichon Frise | Otterhounds American Cocker Spaniel, Greater Swiss Mountain Dog (GSMD), Great Pyrenees, Bichon Frise | [113,114,121,123,124] |
Thrombopathia | RASGRP-1; chr18:52417313-52417315: 3 bp deletion (del TCT) Autosomal recessive procoagulant deficiency at canine chromosome 27 | Basset Hound, Spitz, and cats, Simmental cattle, Greater Swiss Mountain Dog, German Shepherd Dog, Fawn-Hooded (FHwjd) rat | [103,106,108,111,112,115,117,121,122,124,125] |
Thrombocytopenia | Associated with Hashimoto’s lymphocytic thyroiditis (3-5 genes of major histocompatibility complex, MHC, as in humans) | American Cocker Spaniel, Old English Sheepdog, Standard Poodle, Vizsla, Weimaraner, Akita, Samoyed, Shih Tzu, Long -Haired Dachshund, Kerry Blue Terrier, other white/fawn and dilute-color breeds and hybrids | [118,120] |
Macrothrombocytopenia | Norfolk Terrier, Cairn Terrier, Chihuahua, Danish-Swedish Farm Dog, Kritikos Lagonikos, Wesr Highland White Terrier, Parson Russell Terrier, Marenma and Abruzees Sheepdog | [124] |
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Dodds, W.J. One Health: Animal Models of Heritable Human Bleeding Diseases. Animals 2023, 13, 87. https://doi.org/10.3390/ani13010087
Dodds WJ. One Health: Animal Models of Heritable Human Bleeding Diseases. Animals. 2023; 13(1):87. https://doi.org/10.3390/ani13010087
Chicago/Turabian StyleDodds, W. Jean. 2023. "One Health: Animal Models of Heritable Human Bleeding Diseases" Animals 13, no. 1: 87. https://doi.org/10.3390/ani13010087