Genetic Deficiencies of Hyaluronan Degradation
Abstract
:1. Introduction
2. Human Disorders of Hyaluronidase Deficiency
2.1. HYAL1 Deficiency Is the Cause of MPS IX
2.1.1. Phenotype of HYAL1 Deficiency
2.1.2. The Molecular Basis of MPS9
2.1.3. HYAL1 Gene and Protein
2.2. HYAL2 Deficiency Causes Syndromic Cleft Lip and/or Palate
2.2.1. Phenotype of HYAL2 Deficiency
2.2.2. The Molecular Basis of HYAL2-Deficiency
2.2.3. HYAL2 Gene and Protein
2.3. HYAL3 Deficiency and Oligospermia
2.3.1. Phenotype of HYAL3 Deficiency
2.3.2. The Molecular Basis of HYAL3 Deficiency
2.3.3. HYAL3 Gene and Protein
2.4. CEMIP Deficiency
2.4.1. Phenotype of CEMIP Deficiency
2.4.2. The Molecular Basis of CEMIP Deficiency
2.4.3. CEMIP Gene and Protein
3. Murine Models of Hyaluronidase Deficiency
3.1. HYAL1 Deficiency in the Mouse
3.2. HYAL2 Deficiency in the Mouse
3.3. HYAL3 Deficiency in the Mouse
3.4. SPAM1/HYAL5 and HYAL6 Deficiency in the Mouse
3.5. CEMIP Deficiency in the Mouse
3.6. TMEM2 Deficiency in Zebrafish and Mouse Models
4. Summary
Funding
Conflicts of Interest
References
- Ricard-Blum, S.; Vives, R.R.; Schaefer, L.; Gotte, M.; Merline, R.; Passi, A.; Heldin, P.; Magalhaes, A.; Reis, C.A.; Skandalis, S.S.; et al. A biological guide to glycosaminoglycans: Current perspectives and pending questions. FEBS J. 2024. [Google Scholar] [CrossRef] [PubMed]
- Itano, N.; Kimata, K. Mammalian hyaluronan synthases. IUBMB Life 2002, 54, 195–199. [Google Scholar] [CrossRef] [PubMed]
- Maloney, F.P.; Kuklewicz, J.; Corey, R.A.; Bi, Y.; Ho, R.; Mateusiak, L.; Pardon, E.; Steyaert, J.; Stansfeld, P.J.; Zimmer, J. Structure, substrate recognition and initiation of hyaluronan synthase. Nature 2022, 604, 195–201. [Google Scholar] [CrossRef] [PubMed]
- Fraser, J.R.; Laurent, T.C.; Laurent, U.B. Hyaluronan: Its nature, distribution, functions and turnover. J. Intern. Med. 1997, 242, 27–33. [Google Scholar] [CrossRef] [PubMed]
- Fenderson, B.A.; Stamenkovic, I.; Aruffo, A. Localization of hyaluronan in mouse embryos during implantation, gastrulation and organogenesis. Differentiation 1993, 54, 85–98. [Google Scholar] [CrossRef] [PubMed]
- Laurent, T.C.; Fraser, J.R. Hyaluronan. FASEB J. 1992, 6, 2397–2404. [Google Scholar] [CrossRef] [PubMed]
- Fraser, J.R.; Laurent, T.C. Turnover and metabolism of hyaluronan. Ciba Found. Symp. 1989, 143, 41–53, discussion 53–49, 281–285. [Google Scholar] [PubMed]
- Jadin, L.; Bookbinder, L.H.; Frost, G.I. A comprehensive model of hyaluronan turnover in the mouse. Matrix Biol. 2012, 31, 81–89. [Google Scholar] [CrossRef]
- Fraser, J.R.; Kimpton, W.G.; Laurent, T.C.; Cahill, R.N.; Vakakis, N. Uptake and degradation of hyaluronan in lymphatic tissue. Biochem. J. 1988, 256, 153–158. [Google Scholar] [CrossRef]
- Fraser, J.R.; Appelgren, L.E.; Laurent, T.C. Tissue uptake of circulating hyaluronic acid. A whole body autoradiographic study. Cell Tissue Res. 1983, 233, 285–293. [Google Scholar] [CrossRef]
- Roden, L.; Campbell, P.; Fraser, J.R.; Laurent, T.C.; Pertoft, H.; Thompson, J.N. Enzymic pathways of hyaluronan catabolism. Ciba Found. Symp. 1989, 143, 60–76, discussion 76–86, 281–285. [Google Scholar] [CrossRef]
- McBride, K.L.; Flanigan, K.M. Update in the Mucopolysaccharidoses. Semin. Pediatr. Neurol. 2021, 37, 100874. [Google Scholar] [CrossRef]
- Stern, R.; Jedrzejas, M.J. Hyaluronidases: Their genomics, structures, and mechanisms of action. Chem. Rev. 2006, 106, 818–839. [Google Scholar] [CrossRef] [PubMed]
- Gushulak, L.; Hemming, R.; Martin, D.; Seyrantepe, V.; Pshezhetsky, A.; Triggs-Raine, B. Hyaluronidase 1 and beta-hexosaminidase have redundant functions in hyaluronan and chondroitin sulfate degradation. J. Biol. Chem. 2012, 287, 16689–16697. [Google Scholar] [CrossRef]
- Gmachl, M.; Kreil, G. Bee Venom Hyaluronidase Is Homologous to a Membrane-Protein of Mammalian Sperm. Proc. Natl. Acad. Sci. USA 1993, 90, 3569–3573. [Google Scholar] [CrossRef]
- Csoka, A.B.; Frost, G.I.; Heng, H.H.; Scherer, S.W.; Mohapatra, G.; Stern, R. The hyaluronidase gene HYAL1 maps to chromosome 3p21.2-p21.3 in human and 9F1-F2 in mouse, a conserved candidate tumor suppressor locus. Genomics 1998, 48, 63–70. [Google Scholar] [CrossRef] [PubMed]
- Csoka, A.B.; Scherer, S.W.; Stern, R. Expression analysis of six paralogous human hyaluronidase genes clustered on chromosomes 3p21 and 7q31. Genomics 1999, 60, 356–361. [Google Scholar] [CrossRef]
- Triggs-Raine, B.; Salo, T.J.; Zhang, H.; Wicklow, B.A.; Natowicz, M.R. Mutations in HYAL1, a member of a tandemly distributed multigene family encoding disparate hyaluronidase activities, cause a newly described lysosomal disorder, mucopolysaccharidosis IX. Proc. Natl. Acad. Sci. USA 1999, 96, 6296–6300. [Google Scholar] [CrossRef] [PubMed]
- Lepperdinger, G.; Strobl, B.; Kreil, G. HYAL2, a human gene expressed in many cells, encodes a lysosomal hyaluronidase with a novel type of specificity. J. Biol. Chem. 1998, 273, 22466–22470. [Google Scholar] [CrossRef]
- Shuttleworth, T.L.; Wilson, M.D.; Wicklow, B.A.; Wilkins, J.A.; Triggs-Raine, B.L. Characterization of the murine hyaluronidase gene region reveals complex organization and cotranscription of Hyal1 with downstream genes, Fus2 and Hyal3. J. Biol. Chem. 2002, 277, 23008–23018. [Google Scholar] [CrossRef]
- Kim, E.; Baba, D.; Kimura, M.; Yamashita, M.; Kashiwabara, S.; Baba, T. Identification of a hyaluronidase, Hyal5, involved in penetration of mouse sperm through cumulus mass. Proc. Natl. Acad. Sci. USA 2005, 102, 18028–18033. [Google Scholar] [CrossRef] [PubMed]
- Csoka, A.B.; Stern, R. Hypotheses on the evolution of hyaluronan: A highly ironic acid. Glycobiology 2013, 23, 398–411. [Google Scholar] [CrossRef] [PubMed]
- Lerman, M.I.; Minna, J.D. The 630-kb lung cancer homozygous deletion region on human chromosome 3p21.3: Identification and evaluation of the resident candidate tumor suppressor genes. The International Lung Cancer Chromosome 3p21.3 Tumor Suppressor Gene Consortium. Cancer Res. 2000, 60, 6116–6133. [Google Scholar] [PubMed]
- Ji, L.; Nishizaki, M.; Gao, B.; Burbee, D.; Kondo, M.; Kamibayashi, C.; Xu, K.; Yen, N.; Atkinson, E.N.; Fang, B.; et al. Expression of several genes in the human chromosome 3p21.3 homozygous deletion region by an adenovirus vector results in tumor suppressor activities in vitro and in vivo. Cancer Res. 2002, 62, 2715–2720. [Google Scholar] [PubMed]
- Angeloni, D. Molecular analysis of deletions in human chromosome 3p21 and the role of resident cancer genes in disease. Brief. Funct. Genom. Proteomic 2007, 6, 19–39. [Google Scholar] [CrossRef] [PubMed]
- Yoshida, H.; Nagaoka, A.; Kusaka-Kikushima, A.; Tobiishi, M.; Kawabata, K.; Sayo, T.; Sakai, S.; Sugiyama, Y.; Enomoto, H.; Okada, Y.; et al. KIAA1199, a deafness gene of unknown function, is a new hyaluronan binding protein involved in hyaluronan depolymerization. Proc. Natl. Acad. Sci. USA 2013, 110, 5612–5617. [Google Scholar] [CrossRef] [PubMed]
- Yamamoto, H.; Tobisawa, Y.; Inubushi, T.; Irie, F.; Ohyama, C.; Yamaguchi, Y. A mammalian homolog of the zebrafish transmembrane protein 2 (TMEM2) is the long-sought-after cell-surface hyaluronidase. J. Biol. Chem. 2017, 292, 7304–7313. [Google Scholar] [CrossRef] [PubMed]
- Yoshida, H.; Nagaoka, A.; Nakamura, S.; Tobiishi, M.; Sugiyama, Y.; Inoue, S. N-Terminal signal sequence is required for cellular trafficking and hyaluronan-depolymerization of KIAA1199. FEBS Lett. 2014, 588, 111–116. [Google Scholar] [CrossRef] [PubMed]
- Niu, M.; McGrath, M.; Sammon, D.; Gardner, S.; Morgan, R.M.; Di Maio, A.; Liu, Y.; Bubeck, D.; Hohenester, E. Structure of the transmembrane protein 2 (TMEM2) ectodomain and its apparent lack of hyaluronidase activity. Wellcome Open Res. 2023, 8, 76. [Google Scholar] [CrossRef]
- Sato, S.; Miyazaki, M.; Fukuda, S.; Mizutani, Y.; Mizukami, Y.; Higashiyama, S.; Inoue, S. Human TMEM2 is not a catalytic hyaluronidase, but a regulator of hyaluronan metabolism via HYBID (KIAA1199/CEMIP) and HAS2 expression. J. Biol. Chem. 2023, 299, 104826. [Google Scholar] [CrossRef]
- Yamaguchi, Y.; Yamamoto, H.; Tobisawa, Y.; Irie, F. TMEM2: A missing link in hyaluronan catabolism identified? Matrix Biol. 2019, 78–79, 139–146. [Google Scholar] [CrossRef] [PubMed]
- He, Q.Y.; Liu, X.H.; Li, Q.; Studholme, D.J.; Li, X.W.; Liang, S.P. G8: A novel domain associated with polycystic kidney disease and non-syndromic hearing loss. Bioinformatics 2006, 22, 2189–2191. [Google Scholar] [CrossRef] [PubMed]
- Natowicz, M.R.; Short, M.P.; Wang, Y.; Dickersin, G.R.; Gebhardt, M.C.; Rosenthal, D.I.; Sims, K.B.; Rosenberg, A.E. Clinical and biochemical manifestations of hyaluronidase deficiency. N. Engl. J. Med. 1996, 335, 1029–1033. [Google Scholar] [CrossRef] [PubMed]
- Imundo, L.; Leduc, C.A.; Guha, S.; Brown, M.; Perino, G.; Gushulak, L.; Triggs-Raine, B.; Chung, W.K. A complete deficiency of Hyaluronoglucosaminidase 1 (HYAL1) presenting as familial juvenile idiopathic arthritis. J. Inherit. Metab. Dis. 2011, 34, 1013–1022. [Google Scholar] [CrossRef] [PubMed]
- Kiykim, E.; Barut, K.; Cansever, M.S.; Zeybek, C.A.; Zubarioglu, T.; Aydin, A.; Kasapcopur, O. Screening Mucopolysaccharidosis Type IX in Patients with Juvenile Idiopathic Arthritis. JIMD Rep. 2016, 25, 21–24. [Google Scholar] [CrossRef] [PubMed]
- Arming, S.; Strobl, B.; Wechselberger, C.; Kreil, G. In vitro mutagenesis of PH-20 hyaluronidase from human sperm. Eur. J. Biochem./FEBS 1997, 247, 810–814. [Google Scholar] [CrossRef] [PubMed]
- Markovic-Housley, Z.; Miglierini, G.; Soldatova, L.; Rizkallah, P.J.; Muller, U.; Schirmer, T. Crystal structure of hyaluronidase, a major allergen of bee venom. Structure 2000, 8, 1025–1035. [Google Scholar] [CrossRef]
- Meshach Paul, D.; Rajasekaran, R. In silico approach to explore the disruption in the molecular mechanism of human hyaluronidase 1 by mutant E268K that directs Natowicz syndrome. Eur. Biophys. J. 2017, 46, 157–169. [Google Scholar] [CrossRef] [PubMed]
- De Salegui, M.; Plonska, H.; Pigman, W. A comparison of serum and testicular hyaluronidase. Arch. Biochem. Biophys. 1967, 121, 548–554. [Google Scholar] [CrossRef]
- Frost, G.I.; Csoka, A.B.; Wong, T.; Stern, R. Purification, cloning, and expression of human plasma hyaluronidase. Biochem. Biophys. Res. Commun. 1997, 236, 10–15. [Google Scholar] [CrossRef]
- Csoka, A.B.; Frost, G.I.; Wong, T.; Stern, R. Purification and microsequencing of hyaluronidase isozymes from human urine. FEBS Lett. 1997, 417, 307–310. [Google Scholar] [CrossRef] [PubMed]
- Hofinger, E.S.A.; Spickenreither, M.; Oschmann, J.; Bernhardt, G.; Rudolph, R.; Buschauer, A. Recombinant human hyaluronidase Hyal-1:: Insect cells versus as expression system and identification of low molecular weight inhibitors. Glycobiology 2007, 17, 444–453. [Google Scholar] [CrossRef] [PubMed]
- Goto, Y.; Niwa, Y.; Suzuki, T.; Uematsu, S.; Dohmae, N.; Simizu, S. N-glycosylation is required for secretion and enzymatic activity of human hyaluronidase1. FEBS Open Bio 2014, 4, 554–559. [Google Scholar] [CrossRef] [PubMed]
- Chao, K.L.; Muthukumar, L.; Herzberg, O. Structure of human hyaluronidase-1, a hyaluronan hydrolyzing enzyme involved in tumor growth and angiogenesis. Biochemistry 2007, 46, 6911–6920. [Google Scholar] [CrossRef] [PubMed]
- Natowicz, M.R.; Wang, Y. Plasma hyaluronidase activity in mucolipidoses II and III: Marked differences from other lysosomal enzymes. Am. J. Med. Genet. 1996, 65, 209–212. [Google Scholar] [CrossRef]
- Puissant, E.; Gilis, F.; Dogne, S.; Flamion, B.; Jadot, M.; Boonen, M. Subcellular trafficking and activity of Hyal-1 and its processed forms in murine macrophages. Traffic 2014, 15, 500–515. [Google Scholar] [CrossRef] [PubMed]
- Gasingirwa, M.C.; Thirion, J.; Mertens-Strijthagen, J.; Wattiaux-De Coninck, S.; Flamion, B.; Wattiaux, R.; Jadot, M. Endocytosis of hyaluronidase-1 by the liver. Biochem. J. 2010, 430, 305–313. [Google Scholar] [CrossRef] [PubMed]
- Boonen, M.; Puissant, E.; Gilis, F.; Flamion, B.; Jadot, M. Mouse liver lysosomes contain enzymatically active processed forms of Hyal-1. Biochem. Biophys. Res. Commun. 2014, 446, 1155–1160. [Google Scholar] [CrossRef] [PubMed]
- McAtee, C.O.; Berkebile, A.R.; Elowsky, C.G.; Fangman, T.; Barycki, J.J.; Wahl, J.K., 3rd; Khalimonchuk, O.; Naslavsky, N.; Caplan, S.; Simpson, M.A. Hyaluronidase Hyal1 Increases Tumor Cell Proliferation and Motility through Accelerated Vesicle Trafficking. J. Biol. Chem. 2015, 290, 13144–13156. [Google Scholar] [CrossRef]
- Csoka, A.B.; Frost, G.I.; Stern, R. The six hyaluronidase-like genes in the human and mouse genomes. Matrix Biol. 2001, 20, 499–508. [Google Scholar] [CrossRef]
- Fagerberg, L.; Hallstrom, B.M.; Oksvold, P.; Kampf, C.; Djureinovic, D.; Odeberg, J.; Habuka, M.; Tahmasebpoor, S.; Danielsson, A.; Edlund, K.; et al. Analysis of the human tissue-specific expression by genome-wide integration of transcriptomics and antibody-based proteomics. Mol. Cell. Proteom. 2014, 13, 397–406. [Google Scholar] [CrossRef] [PubMed]
- Shaheen, R.; Patel, N.; Shamseldin, H.; Alzahrani, F.; Al-Yamany, R.; Al Moisheer, A.; Ewida, N.; Anazi, S.; Alnemer, M.; Elsheikh, M.; et al. Accelerating matchmaking of novel dysmorphology syndromes through clinical and genomic characterization of a large cohort. Genet. Med. 2016, 18, 686–695. [Google Scholar] [CrossRef] [PubMed]
- Muggenthaler, M.M.; Chowdhury, B.; Hasan, S.N.; Cross, H.E.; Mark, B.; Harlalka, G.V.; Patton, M.A.; Ishida, M.; Behr, E.R.; Sharma, S.; et al. Mutations in HYAL2, Encoding Hyaluronidase 2, Cause a Syndrome of Orofacial Clefting and Cor Triatriatum Sinister in Humans and Mice. PLoS Genet. 2017, 13, e1006470. [Google Scholar] [CrossRef] [PubMed]
- Fasham, J.; Lin, S.; Ghosh, P.; Radio, F.C.; Farrow, E.G.; Thiffault, I.; Kussman, J.; Zhou, D.; Hemming, R.; Zahka, K.; et al. Elucidating the clinical spectrum and molecular basis of HYAL2 deficiency. Genet. Med. 2022, 24, 631–644. [Google Scholar] [CrossRef] [PubMed]
- Strobl, B.; Wechselberger, C.; Beier, D.R.; Lepperdinger, G. Structural organization and chromosomal localization of Hyal2, a gene encoding a lysosomal hyaluronidase. Genomics 1998, 53, 214–219. [Google Scholar] [CrossRef] [PubMed]
- Miller, A.D.; Vigdorovich, V.; Strong, R.K.; Fernandes, R.J.; Lerman, M.I. Hyal2, where are you? Osteoarthr. Cartil. OARS Osteoarthr. Res. Soc. 2006, 14, 1315–1317. [Google Scholar] [CrossRef] [PubMed]
- Andre, B.; Duterme, C.; Van Moer, K.; Mertens-Strijthagen, J.; Jadot, M.; Flamion, B. Hyal2 is a glycosylphosphatidylinositol-anchored, lipid raft-associated hyaluronidase. Biochem. Biophys. Res. Commun. 2011, 411, 175–179. [Google Scholar] [CrossRef] [PubMed]
- Rai, S.K.; Duh, F.M.; Vigdorovich, V.; Danilkovitch-Miagkova, A.; Lerman, M.I.; Miller, A.D. Candidate tumor suppressor HYAL2 is a glycosylphosphatidylinositol (GPI)-anchored cell-surface receptor for jaagsiekte sheep retrovirus, the envelope protein of which mediates oncogenic transformation. Proc. Natl. Acad. Sci. USA 2001, 98, 4443–4448. [Google Scholar] [CrossRef]
- Lepperdinger, G.; Mullegger, J.; Kreil, G. Hyal2--less active, but more versatile? Matrix Biol. 2001, 20, 509–514. [Google Scholar] [CrossRef]
- Bourguignon, L.Y.; Singleton, P.A.; Diedrich, F.; Stern, R.; Gilad, E. CD44 interaction with Na+-H+ exchanger (NHE1) creates acidic microenvironments leading to hyaluronidase-2 and cathepsin B activation and breast tumor cell invasion. J. Biol. Chem. 2004, 279, 26991–27007. [Google Scholar] [CrossRef]
- McCourt, P.A. How does the hyaluronan scrap-yard operate? Matrix Biol. 1999, 18, 427–432. [Google Scholar] [CrossRef] [PubMed]
- Stern, R. Devising a pathway for hyaluronan catabolism: Are we there yet? Glycobiology 2003, 13, 105R–115R. [Google Scholar] [CrossRef] [PubMed]
- Triggs-Raine, B.; Natowicz, M.R. Biology of hyaluronan: Insights from genetic disorders of hyaluronan metabolism. World J. Biol. Chem. 2015, 6, 110–120. [Google Scholar] [CrossRef] [PubMed]
- Hascall, V.; Sandy, J.D.; Handley, C.J. Regulation of proteoglycan metabolism in articular cartilage. In Biology of the Synovial Joint; Archer, C.W., Caterson, B., Eds.; Harwood Academic Publishers: Amsterdam, The Netherlands, 1999; pp. 101–120. [Google Scholar]
- Duterme, C.; Mertens-Strijthagen, J.; Tammi, M.; Flamion, B. Two novel functions of hyaluronidase-2 (Hyal2) are formation of the glycocalyx and control of CD44-ERM interactions. J. Biol. Chem. 2009, 284, 33495–33508. [Google Scholar] [CrossRef] [PubMed]
- Vigdorovich, V.; Strong, R.K.; Miller, A.D. Expression and characterization of a soluble, active form of the jaagsiekte sheep retrovirus receptor, Hyal2. J. Virol. 2005, 79, 79–86. [Google Scholar] [CrossRef] [PubMed]
- de la Motte, C.; Nigro, J.; Vasanji, A.; Rho, H.; Kessler, S.; Bandyopadhyay, S.; Danese, S.; Fiocchi, C.; Stern, R. Platelet-derived hyaluronidase 2 cleaves hyaluronan into fragments that trigger monocyte-mediated production of proinflammatory cytokines. Am. J. Pathol. 2009, 174, 2254–2264. [Google Scholar] [CrossRef] [PubMed]
- Albeiroti, S.; Ayasoufi, K.; Hill, D.R.; Shen, B.; de la Motte, C.A. Platelet hyaluronidase-2: An enzyme that translocates to the surface upon activation to function in extracellular matrix degradation. Blood 2015, 125, 1460–1469. [Google Scholar] [CrossRef] [PubMed]
- Aslam, S.; Zhang, Z.; Latif, Z. Identification of novel homozygous missense and deletion mutations manifesting oligospermia infertility in Kashmiri population. J. Gene Med. 2024, 26, e3589. [Google Scholar] [CrossRef] [PubMed]
- Reese, K.L.; Aravindan, R.G.; Griffiths, G.S.; Shao, M.; Wang, Y.; Galileo, D.S.; Atmuri, V.; Triggs-Raine, B.L.; Martin-Deleon, P.A. Acidic hyaluronidase activity is present in mouse sperm and is reduced in the absence of SPAM1: Evidence for a role for hyaluronidase 3 in mouse and human sperm. Mol. Reprod. Dev. 2010, 77, 759–772. [Google Scholar] [CrossRef]
- Abe, S.; Usami, S.; Nakamura, Y. Mutations in the gene encoding KIAA1199 protein, an inner-ear protein expressed in Deiters’ cells and the fibrocytes, as the cause of nonsyndromic hearing loss. J. Hum. Genet. 2003, 48, 564–570. [Google Scholar] [CrossRef]
- Usami, S.; Wagatsuma, M.; Fukuoka, H.; Suzuki, H.; Tsukada, K.; Nishio, S.; Takumi, Y.; Abe, S. The responsible genes in Japanese deafness patients and clinical application using Invader assay. Acta Otolaryngol. 2008, 128, 446–454. [Google Scholar] [CrossRef] [PubMed]
- Zhai, X.; Wang, W.; Ma, Y.; Zeng, Y.; Dou, D.; Fan, H.; Song, J.; Yu, X.; Xin, D.; Du, G.; et al. Serum KIAA1199 is an advanced-stage prognostic biomarker and metastatic oncogene in cholangiocarcinoma. Aging 2020, 12, 23761–23777. [Google Scholar] [CrossRef] [PubMed]
- Tiwari, A.; Schneider, M.; Fiorino, A.; Haider, R.; Okoniewski, M.J.; Roschitzki, B.; Uzozie, A.; Menigatti, M.; Jiricny, J.; Marra, G. Early insights into the function of KIAA1199, a markedly overexpressed protein in human colorectal tumors. PLoS ONE 2013, 8, e69473. [Google Scholar] [CrossRef] [PubMed]
- Fink, S.P.; Myeroff, L.L.; Kariv, R.; Platzer, P.; Xin, B.; Mikkola, D.; Lawrence, E.; Morris, N.; Nosrati, A.; Willson, J.K.; et al. Induction of KIAA1199/CEMIP is associated with colon cancer phenotype and poor patient survival. Oncotarget 2015, 6, 30500–30515. [Google Scholar] [CrossRef] [PubMed]
- Rodrigues, G.; Hoshino, A.; Kenific, C.M.; Matei, I.R.; Steiner, L.; Freitas, D.; Kim, H.S.; Oxley, P.R.; Scandariato, I.; Casanova-Salas, I.; et al. Tumour exosomal CEMIP protein promotes cancer cell colonization in brain metastasis. Nat. Cell Biol. 2019, 21, 1403–1412. [Google Scholar] [CrossRef] [PubMed]
- Kuwabara, N.; Manya, H.; Yamada, T.; Tateno, H.; Kanagawa, M.; Kobayashi, K.; Akasaka-Manya, K.; Hirose, Y.; Mizuno, M.; Ikeguchi, M.; et al. Carbohydrate-binding domain of the POMGnT1 stem region modulates O-mannosylation sites of alpha-dystroglycan. Proc. Natl. Acad. Sci. USA 2016, 113, 9280–9285. [Google Scholar] [CrossRef] [PubMed]
- Usami, S.; Takumi, Y.; Suzuki, N.; Oguchi, T.; Oshima, A.; Suzuki, H.; Kitoh, R.; Abe, S.; Sasaki, A.; Matsubara, A. The localization of proteins encoded by CRYM, KIAA1199, UBA52, COL9A3, and COL9A1, genes highly expressed in the cochlea. Neuroscience 2008, 154, 22–28. [Google Scholar] [CrossRef] [PubMed]
- Michishita, E.; Garces, G.; Barrett, J.C.; Horikawa, I. Upregulation of the KIAA1199 gene is associated with cellular mortality. Cancer Lett. 2006, 239, 71–77. [Google Scholar] [CrossRef] [PubMed]
- Terashima, M.; Fujita, Y.; Togashi, Y.; Sakai, K.; De Velasco, M.A.; Tomida, S.; Nishio, K. KIAA1199 interacts with glycogen phosphorylase kinase beta-subunit (PHKB) to promote glycogen breakdown and cancer cell survival. Oncotarget 2014, 5, 7040–7050. [Google Scholar] [CrossRef]
- Zhang, Y.; Jia, S.; Jiang, W.G. KIAA1199 and its biological role in human cancer and cancer cells (review). Oncol. Rep. 2014, 31, 1503–1508. [Google Scholar] [CrossRef]
- Domanegg, K.; Sleeman, J.P.; Schmaus, A. CEMIP, a Promising Biomarker That Promotes the Progression and Metastasis of Colorectal and Other Types of Cancer. Cancers 2022, 14, 5093. [Google Scholar] [CrossRef] [PubMed]
- Evensen, N.A.; Kuscu, C.; Nguyen, H.L.; Zarrabi, K.; Dufour, A.; Kadam, P.; Hu, Y.J.; Pulkoski-Gross, A.; Bahou, W.F.; Zucker, S.; et al. Unraveling the role of KIAA1199, a novel endoplasmic reticulum protein, in cancer cell migration. J. Natl. Cancer Inst. 2013, 105, 1402–1416. [Google Scholar] [CrossRef] [PubMed]
- Duong, H.Q.; Nemazanyy, I.; Rambow, F.; Tang, S.C.; Delaunay, S.; Tharun, L.; Florin, A.; Buttner, R.; Vandaele, D.; Close, P.; et al. The Endosomal Protein CEMIP Links WNT Signaling to MEK1-ERK1/2 Activation in Selumetinib-Resistant Intestinal Organoids. Cancer Res. 2018, 78, 4533–4548. [Google Scholar] [CrossRef] [PubMed]
- Birkenkamp-Demtroder, K.; Maghnouj, A.; Mansilla, F.; Thorsen, K.; Andersen, C.L.; Oster, B.; Hahn, S.; Orntoft, T.F. Repression of KIAA1199 attenuates Wnt-signalling and decreases the proliferation of colon cancer cells. Br. J. Cancer 2011, 105, 552–561. [Google Scholar] [CrossRef] [PubMed]
- Yamada, S.; Mizumoto, S. Characterization of Hyaluronidase 4 Involved in the Catabolism of Chondroitin Sulfate. Molecules 2022, 27, 6103. [Google Scholar] [CrossRef] [PubMed]
- Martin, D.C.; Atmuri, V.; Hemming, R.J.; Farley, J.; Mort, J.S.; Byers, S.; Hombach-Klonisch, S.; Csoka, A.B.; Stern, R.; Triggs-Raine, B.L. A mouse model of human mucopolysaccharidosis IX exhibits osteoarthritis. Hum. Mol. Genet. 2008, 17, 1904–1915. [Google Scholar] [CrossRef] [PubMed]
- Puissant, E.; Gilis, F.; Tevel, V.; Vandeweerd, J.M.; Flamion, B.; Jadot, M.; Boonen, M. Hyaluronidase 1 deficiency decreases bone mineral density in mice. Sci. Rep. 2022, 12, 10142. [Google Scholar] [CrossRef] [PubMed]
- Bourguignon, V.; Flamion, B. Respective roles of hyaluronidases 1 and 2 in endogenous hyaluronan turnover. FASEB J. 2016, 30, 2108–2114. [Google Scholar] [CrossRef] [PubMed]
- Colombaro, V.; Jadot, I.; Decleves, A.E.; Voisin, V.; Giordano, L.; Habsch, I.; Flamion, B.; Caron, N. Hyaluronidase 1 and hyaluronidase 2 are required for renal hyaluronan turnover. Acta Histochem. 2015, 117, 83–91. [Google Scholar] [CrossRef]
- Malaisse, J.; Evrard, C.; Feret, D.; Colombaro, V.; Dogne, S.; Haftek, M.; de Rouvroit, C.L.; Flamion, B.; Poumay, Y. Hyaluronidase-1 Is Mainly Functional in the Upper Granular Layer, Close to the Epidermal Barrier. J. Investig. Dermatol. 2015, 135, 3189–3192. [Google Scholar] [CrossRef]
- Dumaresq-Doiron, K.; Edjekouane, L.; Orimoto, A.M.; Yoffou, P.H.; Gushulak, L.; Triggs-Raine, B.; Carmona, E. Hyal-1 but not Hyal-3 deficiency has an impact on ovarian folliculogenesis and female fertility by altering the follistatin/activin/Smad3 pathway and the apoptotic process. J. Cell. Physiol. 2012, 227, 1911–1922. [Google Scholar] [CrossRef] [PubMed]
- Sango, K.; McDonald, M.P.; Crawley, J.N.; Mack, M.L.; Tifft, C.J.; Skop, E.; Starr, C.M.; Hoffmann, A.; Sandhoff, K.; Suzuki, K.; et al. Mice lacking both subunits of lysosomal beta-hexosaminidase display gangliosidosis and mucopolysaccharidosis. Nat. Genet. 1996, 14, 348–352. [Google Scholar] [CrossRef]
- Suzuki, K.; Sango, K.; Proia, R.L.; Langaman, C. Mice deficient in all forms of lysosomal beta-hexosaminidase show mucopolysaccharidosis-like pathology. J. Neuropathol. Exp. Neurol. 1997, 56, 693–703. [Google Scholar] [CrossRef]
- Jadin, L.; Wu, X.; Ding, H.; Frost, G.I.; Onclinx, C.; Triggs-Raine, B.; Flamion, B. Skeletal and hematological anomalies in HYAL2-deficient mice: A second type of mucopolysaccharidosis IX? FASEB J. 2008, 22, 4316–4326. [Google Scholar] [CrossRef] [PubMed]
- Chowdhury, B.; Hemming, R.; Hombach-Klonisch, S.; Flamion, B.; Triggs-Raine, B. Murine hyaluronidase 2 deficiency results in extracellular hyaluronan accumulation and severe cardiopulmonary dysfunction. J. Biol. Chem. 2013, 288, 520–528. [Google Scholar] [CrossRef]
- Chowdhury, B.; Hemming, R.; Faiyaz, S.; Triggs-Raine, B. Hyaluronidase 2 (HYAL2) is expressed in endothelial cells, as well as some specialized epithelial cells, and is required for normal hyaluronan catabolism. Histochem. Cell Biol. 2016, 145, 53–66. [Google Scholar] [CrossRef]
- Onclinx, C.; Dogne, S.; Jadin, L.; Andris, F.; Grandfils, C.; Jouret, F.; Mullier, F.; Flamion, B. Deficiency in mouse hyaluronidase 2: A new mechanism of chronic thrombotic microangiopathy. Haematologica 2015, 100, 1023–1030. [Google Scholar] [CrossRef]
- Chowdhury, B.; Xiang, B.; Muggenthaler, M.; Dolinsky, V.W.; Triggs-Raine, B. Hyaluronidase 2 deficiency is a molecular cause of cor triatriatum sinister in mice. Int. J. Cardiol. 2016, 209, 281–283. [Google Scholar] [CrossRef] [PubMed]
- Chowdhury, B.; Xiang, B.; Liu, M.; Hemming, R.; Dolinsky, V.W.; Triggs-Raine, B. Hyaluronidase 2 Deficiency Causes Increased Mesenchymal Cells, Congenital Heart Defects, and Heart Failure. Circ. Cardiovasc. Genet. 2017, 10, e001598. [Google Scholar] [CrossRef]
- Higuchi, Y.; Nishida, Y.; Kozawa, E.; Zhuo, L.; Arai, E.; Hamada, S.; Morita, D.; Ikuta, K.; Kimata, K.; Ushida, T.; et al. Conditional knockdown of hyaluronidase 2 in articular cartilage stimulates osteoarthritic progression in a mice model. Sci. Rep. 2017, 7, 7028. [Google Scholar] [CrossRef]
- Atmuri, V.; Martin, D.C.; Hemming, R.; Gutsol, A.; Byers, S.; Sahebjam, S.; Thliveris, J.A.; Mort, J.S.; Carmona, E.; Anderson, J.E.; et al. Hyaluronidase 3 (HYAL3) knockout mice do not display evidence of hyaluronan accumulation. Matrix Biol. 2008, 27, 653–660. [Google Scholar] [CrossRef]
- Hemming, R.; Martin, D.C.; Slominski, E.; Nagy, J.I.; Halayko, A.J.; Pind, S.; Triggs-Raine, B. Mouse Hyal3 encodes a 45–56 kDa glycoprotein whose overexpression increases hyaluronidase 1 activity in cultured cells. Glycobiology 2008, 18, 280–289. [Google Scholar] [CrossRef] [PubMed]
- Cherr, G.N.; Yudin, A.I.; Overstreet, J.W. The dual functions of GPI-anchored PH-20: Hyaluronidase and intracellular signaling. Matrix Biol. 2001, 20, 515–525. [Google Scholar] [CrossRef] [PubMed]
- Baba, D.; Kashiwabara, S.I.; Honda, A.; Yamagata, K.; Wu, Q.; Ikawa, M.; Okabe, M.; Baba, T. Mouse sperm lacking cell surface hyaluronidase PH-20 can pass through the layer of cumulus cells and fertilize the egg. J. Biol. Chem. 2002, 277, 30310–30314. [Google Scholar] [CrossRef] [PubMed]
- Park, S.; Kim, Y.H.; Jeong, P.S.; Park, C.; Lee, J.W.; Kim, J.S.; Wee, G.; Song, B.S.; Park, B.J.; Kim, S.H.; et al. SPAM1/HYAL5 double deficiency in male mice leads to severe male subfertility caused by a cumulus-oocyte complex penetration defect. FASEB J. 2019, 33, 14440–14449. [Google Scholar] [CrossRef] [PubMed]
- Bang, H.; Lee, S.; Jeong, P.S.; Seol, D.W.; Son, D.; Kim, Y.H.; Song, B.S.; Sim, B.W.; Park, S.; Lee, D.M.; et al. Hyaluronidase 6 Does Not Affect Cumulus-Oocyte Complex Dispersal and Male Mice Fertility. Genes 2022, 13, 753. [Google Scholar] [CrossRef] [PubMed]
- Shimoda, M.; Yoshida, H.; Mizuno, S.; Hirozane, T.; Horiuchi, K.; Yoshino, Y.; Hara, H.; Kanai, Y.; Inoue, S.; Ishijima, M.; et al. Hyaluronan-Binding Protein Involved in Hyaluronan Depolymerization Controls Endochondral Ossification through Hyaluronan Metabolism. Am. J. Pathol. 2017, 187, 1162–1176. [Google Scholar] [CrossRef]
- Chen, L.; Shi, K.; Ditzel, N.; Qiu, W.; Figeac, F.; Nielsen, L.H.D.; Tencerova, M.; Kowal, J.M.; Ding, M.; Andreasen, C.M.; et al. KIAA1199 deficiency enhances skeletal stem cell differentiation to osteoblasts and promotes bone regeneration. Nat. Commun. 2023, 14, 2016. [Google Scholar] [CrossRef] [PubMed]
- Momoeda, M.; de Vega, S.; Kaneko, H.; Yoshinaga, C.; Shimoda, M.; Nakamura, T.; Endo, Y.; Yoshida, H.; Kaneko, K.; Ishijima, M.; et al. Deletion of Hyaluronan-Binding Protein Involved in Hyaluronan Depolymerization (HYBID) Results in Attenuation of Osteoarthritis in Mice. Am. J. Pathol. 2021, 191, 1986–1998. [Google Scholar] [CrossRef]
- Yoshino, Y.; Ishisaka, M.; Tsuruma, K.; Shimazawa, M.; Yoshida, H.; Inoue, S.; Shimoda, M.; Okada, Y.; Hara, H. Distribution and function of hyaluronan binding protein involved in hyaluronan depolymerization (HYBID, KIAA1199) in the mouse central nervous system. Neuroscience 2017, 347, 1–10. [Google Scholar] [CrossRef]
- Yoshino, Y.; Shimazawa, M.; Nakamura, S.; Inoue, S.; Yoshida, H.; Shimoda, M.; Okada, Y.; Hara, H. Targeted deletion of HYBID (hyaluronan binding protein involved in hyaluronan depolymerization/ KIAA1199/CEMIP) decreases dendritic spine density in the dentate gyrus through hyaluronan accumulation. Biochem. Biophys. Res. Commun. 2018, 503, 1934–1940. [Google Scholar] [CrossRef] [PubMed]
- Dokoshi, T.; Zhang, L.J.; Li, F.; Nakatsuji, T.; Butcher, A.; Yoshida, H.; Shimoda, M.; Okada, Y.; Gallo, R.L. Hyaluronan Degradation by Cemip Regulates Host Defense against Staphylococcus aureus Skin Infection. Cell Rep. 2020, 30, 61–68.e64. [Google Scholar] [CrossRef] [PubMed]
- Peters, A.; Sherman, L.S. Diverse Roles for Hyaluronan and Hyaluronan Receptors in the Developing and Adult Nervous System. Int. J. Mol. Sci. 2020, 21, 5988. [Google Scholar] [CrossRef] [PubMed]
- Arranz, A.M.; Perkins, K.L.; Irie, F.; Lewis, D.P.; Hrabe, J.; Xiao, F.; Itano, N.; Kimata, K.; Hrabetova, S.; Yamaguchi, Y. Hyaluronan deficiency due to Has3 knock-out causes altered neuronal activity and seizures via reduction in brain extracellular space. J. Neurosci. 2014, 34, 6164–6176. [Google Scholar] [CrossRef] [PubMed]
- Smith, K.A.; Lagendijk, A.K.; Courtney, A.D.; Chen, H.; Paterson, S.; Hogan, B.M.; Wicking, C.; Bakkers, J. Transmembrane protein 2 (Tmem2) is required to regionally restrict atrioventricular canal boundary and endocardial cushion development. Development 2011, 138, 4193–4198. [Google Scholar] [CrossRef]
- De Angelis, J.E.; Lagendijk, A.K.; Chen, H.; Tromp, A.; Bower, N.I.; Tunny, K.A.; Brooks, A.J.; Bakkers, J.; Francois, M.; Yap, A.S.; et al. Tmem2 Regulates Embryonic Vegf Signaling by Controlling Hyaluronic Acid Turnover. Dev. Cell 2017, 40, 421. [Google Scholar] [CrossRef] [PubMed]
- Ryckebusch, L.; Hernandez, L.; Wang, C.; Phan, J.; Yelon, D. Tmem2 regulates cell-matrix interactions that are essential for muscle fiber attachment. Development 2016, 143, 2965–2972. [Google Scholar] [CrossRef] [PubMed]
- Hernandez, L.; Ryckebusch, L.; Wang, C.; Ling, R.; Yelon, D. Tmem2 restricts atrioventricular canal differentiation by regulating degradation of hyaluronic acid. Dev. Dyn. 2019, 248, 1195–1210. [Google Scholar] [CrossRef] [PubMed]
- Narita, T.; Tobisawa, Y.; Bobkov, A.; Jackson, M.; Ohyama, C.; Irie, F.; Yamaguchi, Y. TMEM2 is a bona fide hyaluronidase possessing intrinsic catalytic activity. J. Biol. Chem. 2023, 299, 105120. [Google Scholar] [CrossRef]
- Tobisawa, Y.; Fujita, N.; Yamamoto, H.; Ohyama, C.; Irie, F.; Yamaguchi, Y. The cell surface hyaluronidase TMEM2 is essential for systemic hyaluronan catabolism and turnover. J. Biol. Chem. 2021, 297, 101281. [Google Scholar] [CrossRef]
- Inubushi, T.; Nakanishi, Y.; Abe, M.; Takahata, Y.; Nishimura, R.; Kurosaka, H.; Irie, F.; Yamashiro, T.; Yamaguchi, Y. The cell surface hyaluronidase TMEM2 plays an essential role in mouse neural crest cell development and survival. PLoS Genet. 2022, 18, e1009765. [Google Scholar] [CrossRef] [PubMed]
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Fink, S.P.; Triggs-Raine, B. Genetic Deficiencies of Hyaluronan Degradation. Cells 2024, 13, 1203. https://doi.org/10.3390/cells13141203
Fink SP, Triggs-Raine B. Genetic Deficiencies of Hyaluronan Degradation. Cells. 2024; 13(14):1203. https://doi.org/10.3390/cells13141203
Chicago/Turabian StyleFink, Stephen P., and Barbara Triggs-Raine. 2024. "Genetic Deficiencies of Hyaluronan Degradation" Cells 13, no. 14: 1203. https://doi.org/10.3390/cells13141203