Characterization of PCLO Gene in Amazonian Native American Populations
Abstract
:1. Introduction
2. Materials and Methods
2.1. Study Populations
2.2. Extraction of the DNA and Preparation of the Exome Library
2.3. Bioinformatic Analysis
2.4. Statistical Analyses
3. Results
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Fenster, S.D.; Kessels, M.M.; Qualmann, B.; Chung, W.J.; Nash, J.; Gundelfinger, E.D.; Garner, C.C. Interactions between Piccolo and the actin/dynamin-binding protein Abp1 link vesicle endocytosis to presynaptic active zones. J. Biol. Chem. 2003, 278, 20268–20277. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Limbach, C.; Laue, M.M.; Wang, X.; Hu, B.; Thiede, N.; Hultqvist, G.; Kilimanne, M.W. Molecular in situ topology of Aczonin/Piccolo and associated proteins at the mammalian neurotransmitter release site. Proc. Natl. Acad. Sci. USA 2011, 108, E392–E401. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Minelli, A.; Scassellati, C.; Cloninger, C.R.; Tessari, E.; Bortolomasi, M.; Bonvicini, C.; Giacopuzzi, M.; Frisoni, G.B.; Gennarelli, M. PCLO gene: Its role in vulnerability to major depressive disorder. J. Affect. Disord. 2012, 139, 250–255. [Google Scholar] [CrossRef] [PubMed]
- Schuhmacher, A.; Mo¨ssner, R.; Ho¨fels, S.; Pfeiffer, U.; Guttenthaler, V.; Wagner, M.; Schwab, S.G.; Maier, W.; Zobel, A. PCLO rs2522833 modulates HPA system response to antidepressant treatment in major depressive disorder. Int. J. Neuropsychopharmacol. 2011, 14, 237–245. [Google Scholar] [CrossRef] [PubMed]
- Zhang, W.; Hong, R.; Xue, L.; Ou, Y.; Liu, X.; Zhao, Z.; Xiao, W.; Dong, D.; Dong, L.; Fu, M.; et al. Piccolo mediates EGFR signaling and acts as a prognostic biomarker in esophageal squamous cell carcinoma. Oncogene 2017, 36, 3890–3902. [Google Scholar] [CrossRef] [PubMed]
- Waites, C.L.; Leal-Ortiz, S.A.; Okerlund, N.; Dalke, H.; Fejtova, A.; Altrock, W.D.; Gundelfinger, E.D.; Garner, C.C. Bassoon and Piccolo maintain synapse integrity by regulating protein ubiquitination and degradation. EMBO J. 2013, 32, 954–969. [Google Scholar] [CrossRef] [Green Version]
- Gundelfinger, E.D.; Reissner, C.; Garner, C.C. Role of Bassoon and Piccolo in Assembly and Molecular Organization of the Active Zone. Front. Synaptic Neurosci. 2015, 7, 19. [Google Scholar] [CrossRef] [Green Version]
- Ivanova, D.; Dirks, A.; Montenegro-Venegas, C.; Schöne, C.; Altrock, W.D.; Marini, C.; Frischknecht, R.; Schanze, D.; Zenker, M.; Gundelfinger, E.D. Synaptic activity controls localization and function of CtBP1 via binding to Bassoon and Piccolo. EMBO J. 2015, 34, 1056–1077. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sullivan, P.F.; Geus, E.J.C.; Willemsen, G.; James, M.R.; Smit, J.H.; Zandbelt, T.; Arolt, V.; Baune, B.T.; Blackwood, D.; Cichon, S.; et al. Genome-wide association for major depressive disorder: A possible role for the presynaptic protein piccolo. Mol. Psychiatry 2009, 14, 359–375. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Shadrina, M.; Bondarenko, E.A.; Slominsky, P.A. Genetics Factors in Major Depression Disease. Front. Psychiatry 2018, 9, 334. [Google Scholar] [CrossRef] [Green Version]
- Choi, K.H.; Higgs, B.W.; Wendland, J.R.; Song, J.; McMahon, F.J.; Webster, M.J. Gene Expression and Genetic Variation Data Implicate PCLO in Bipolar Disorder. Biol. Psychiatry. 2011, 69, 353. [Google Scholar] [CrossRef] [Green Version]
- Fujimoto, K.; Shibasaki, T.; Yokoi, N.; Kashima, Y.; Matsumoto, M.; Sasaki, T.; Tajima, N.; Iwanaga, T.; Seino, S. Piccolo, a Ca2+ sensor in pancreatic beta-cells: Involvement of cAMP-GEFII.Rim2. Piccolo complex in cAMP-dependent exocytosis. J. Biol. Chem. 2002, 277, 50497–50502. [Google Scholar] [CrossRef] [Green Version]
- Ma, L.; Hanson, R.L.; Que, L.N.; Guo, Y.; Kobes, S.; Bogardus, C.; Baier, L.J. PCLO Variants Are Nominally Associated with Early-Onset Type 2 Diabetes and Insulin Resistance in Pima Indians. Diabetes 2008, 57, 3156–3160. [Google Scholar] [CrossRef] [Green Version]
- Brasil Indígena. Available online: https://indigenas.ibge.gov.br/images/pdf/indigenas/folder_indigenas_web.pdf (accessed on 26 April 2021).
- Cuautle-Rodríguez, P.; Llerena, A.; Molina-Guarneros, J. Present status and perspective of pharmacogenetics in Mexico. Drug Metab. Drug Interact. 2014, 29, 37–45. [Google Scholar] [CrossRef]
- Pinto, P.; Salgado, C.; Santos, N.P.C.; Santos, S.; Ribeiro-dos-Santos, Â. Influence of Genetic Ancestry on INDEL Markers of NFKβ1, CASP8, PAR1, IL4 and CYP19A1 Genes in Leprosy Patients. PLoS Negl. Trop. Dis. 2015, 9, e0004050. [Google Scholar] [CrossRef] [Green Version]
- Carvalho, D.C.; Wanderley, A.V.; Dos Santos, A.M.R.; Moreira, F.C.; de Sá, R.B.A.; Fernandes, M.R.; Modesto, A.A.C.; de Souza, T.P.; Cohen-Paes, A.; Leitão, L.P.C.; et al. Characterization of pharmacogenetic markers related to Acute Lymphoblastic Leukemia toxicity in Amazonian native Americans population. Sci. Rep. 2020, 10, 10292. [Google Scholar] [CrossRef]
- Leal, D.F.V.B.; Silva, M.N.S.; Fernandes, D.C.R.O.; Rodrigues, J.C.G.; Barros, M.C.C.; Pinto, P.D.C.; Pastana, L.F.; Silva, C.A.; Fernandes, M.R.; Assumpção, P.P.; et al. Amerindian genetic ancestry as a risk factor for tuberculosis in an amazonian population. PLoS ONE 2020, 16, e0236033. [Google Scholar] [CrossRef]
- Sambrook, J.; Green, M.R. Molecular Cloning: A Laboratory Manual, 4th ed.; Cold Spring Harbor Laboratory Press: Cold Spring Harbor, NY, USA, 2012. [Google Scholar]
- Benjamini, Y.; Hochberg, Y. Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing. J. R. Stat. Soc. 1995, 57, 289–300. [Google Scholar] [CrossRef]
- Cases-Langhoff, C.; Voss, B.; Garner, A.M.; Appeltauer, U.; Takei, K.; Kindler, S.; Veh, R.W.; De Camilli, P.; Gundelfinger, E.D.; Garner, C.C. Piccolo, a novel 420 kDa protein associated with the presynaptic cytomatrix. Eur. J. Cell Biol. 1996, 69, 214–223. [Google Scholar]
- Rubin, G.M.; Yandell, M.D.; Wortman, J.R.; Gabor, G.L.; Nelson, C.R.; Hariharan, I.K.; Fortini, M.E.; Li, P.W.; Apweiler, R.; Fleischmann, W.; et al. Comparative genomics of the eukaryotes. Science 2000, 287, 2204–2215. [Google Scholar] [CrossRef] [Green Version]
- Ahmed, M.Y.; Chioza, B.A.; Rajab, A.; Schmitz-Abe, K.; Al-Khayat, A.; Al-Turki, S.; Baple, E.L.; Patton, M.A.; Al-Memar, A.Y.; Hurles, M.E. Loss of PCLO function underlies pontocerebellar hypoplasia type III. Neurology 2015, 84, 1745–1750. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bochdanovits, Z.; Verhage, M.; Smit, A.B.; de Geus, E.J.; Posthuma, D.; Boomsma, D.I.; Penninx, B.W.; Hoogendijk, W.J.; Heutink, P. Joint reanalysis of 29 correlated SNPs supports the role of PCLO/Piccolo as a causal risk factor for major depressive disorder. Mol. Psychiatry 2009, 14, 650–652. [Google Scholar] [CrossRef] [PubMed]
- Salzano, F.M. Genetic diversity of South American human populations at the DNA and protein levels. J. Exp. Zool. 1998, 282, 157–163. [Google Scholar] [CrossRef]
- Ribeiro-dos-Santos, A.M.; de Souza, J.E.; Almeida, R.; Alencar, D.O.; Barbosa, M.S.; Gusmão, L.; Silva, W.A., Jr.; de Souza, S.J.; Silva, A.; Ribeiro-dos-Santos, Â.; et al. High-Throughput Sequencing of a South American Amerindian. PLoS ONE 2013, 8, e83340. [Google Scholar] [CrossRef] [Green Version]
- Rodrigues, J.C.G.; Fernandes, M.R.; Guerreiro, J.F.; da Silva, A.L.D.C.; Ribeiro-Dos-Santos, Â.; Santos, S.; Santos, N.P.C.D. Polymorphisms of ADME-related genes and their implications for drug safety and efficacy in Amazonian Amerindians. Sci. Rep. 2019, 9, 7201. [Google Scholar] [CrossRef] [PubMed]
- Rodrigues, J.C.G.; Souza, T.P.; Pastana, L.F.; Ribeiro Dos Santos, A.M.; Fernandes, M.R.; Pinto, P.; Wanderley, A.V.; Souza, S.J.; Kroll, J.E.; Pereira, A.L.; et al. Identification of NUDT15 gene variants in Amazonian Amerindians and admixed individuals from northern Brazil. PLoS ONE 2020, 15, e0231651. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Dobbin, E.A.F.; Medeiros, J.A.G.; Costa, M.S.C.R.; Rodrigues, J.C.G.; Guerreiro, J.F.; Kroll, J.E.; Souza, S.J.; Assumpcao, P.P.; Ribeiro-Dos-Santos, A.K.C.; Santos, S.E.; et al. Identification of Variants (rs11571707, rs144848, and rs11571769] in the BRCA2 Gene Associated with Hereditary Breast Cancer in Indigenous Populations of the Brazilian Amazon. Genes 2021, 12, 142. [Google Scholar] [CrossRef] [PubMed]
- Kittles, R.A.; Chen, W.; Panguluri, R.K.; Ahaghotu, C.; Jackson, A.; Adebamowo, C.A.; Griffin, R.; Williams, T.; Ukoli, F.; Adams-Campbell, L.; et al. CYP3A4-V and prostate cancer in African Americans: Causal or confounding association because of population stratification? Hum. Genet. 2002, 110, 553–560. [Google Scholar] [CrossRef]
- Skoglund, P.; Reich, D. A genomic view of the peopling of the Americas. Curr. Opin. Genet. Dev. 2016, 41, 27–35. [Google Scholar] [CrossRef] [Green Version]
- Wang, S.; Lewis, C.M., Jr.; Jakobsson, M.; Ramachandran, S.; Ray, N.; Bedoya, G.; Rojas, W.; Parra, M.V.; Molina, J.A.; Gallo, C.; et al. Genetic Variation and Population Structure in Native Americans. PLoS Genet. 2007, 3, e185. [Google Scholar] [CrossRef]
- Santos, N.P.; Ribeiro-Rodrigues, E.M.; Ribeiro-Dos-Santos, A.K.; Pereira, R.; Gusmão, L.; Amorim, A.; Guerreiro, J.F.; Zago, M.A.; Matte, C.; Hutz, M.H.; et al. Assessing individual interethnic admixture and population substructure using a 48–insertion-deletion (INSEL) ancestry-informative marker (AIM) panel. Hum. Mutat. 2010, 31, 184–190. [Google Scholar] [CrossRef] [PubMed]
- Amador, M.A.; Cavalcante, G.C.; Santos, N.P.; Gusmão, L.; Guerreiro, J.F.; Ribeirodos-Santos, Â.; Santos, S. Distribution of allelic and genotypic frequencies of IL1A, IL4, NFKB1 and PAR1 variants in Native American, African, European and Brazilian populations. BMC Res. Notes 2016, 9, 101. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Cavalli-Sforza, L.L.; Menozzi, P.; Piazza, A. The History and Geography of Human Genes, 1st ed.; Princeton University Press: Princeton, NJ, USA, 1994. [Google Scholar]
- Jobling, M.A.; Hurles, M.E.; Tyler-Smith, C. Human Evolutionary Genetics: Origins, Peoples & Disease; Garland Science: New York, NY, USA, 2004. [Google Scholar]
Genomic Position | SNP Identification (SNP ID) | Nucleotide Change | Impact Predicted by SNPeff | Variant Type |
---|---|---|---|---|
7:82915671 | rs17156844 | A > G | Low | SNV |
7:82826579 | rs2715150 | A > G | Modifier | SNV |
7:83135105 | rs550369696 | T > C | Low | SNV |
7:83155781 | rs61741659 | T > C | Moderate | SNV |
7:83135109 | rs2877 | C > G | Moderate | SNV |
7:83155515 | rs762371134 | T > GTG | Moderate | INDEL |
7:82952543 | rs976714 | C > T | Moderate | SNV |
7:82952172 | rs10630259 | T > TTCA | Moderate | INDEL |
7:82824392 | rs2522833 | A > C | Moderate | SNV |
7:82953530 | rs10954696 | C > T | Moderate | SNV |
7:82952942 | rs10261848 | T > G | Moderate | SNV |
7:82951497 | rs76988622 | T > C | Low | SNV |
7:82966426 | rs28680905 | T > C | Moderate | SNV |
7:82902684 | rs182078347 | T > C | Moderate | SNV |
7:82966518 | rs6963292 | G > A | Modifier | SNV |
7:82953100 | rs377241009 | G > T | Moderate | SNV |
7:82953964 | rs17148149 | C > T | Moderate | SNV |
7:82805717 | rs12668093 | C > T | Low | SNV |
SNP ID | AMR | AFR | EAS | EUR | SAS | NAT | ABraOM |
---|---|---|---|---|---|---|---|
rs17156844 | 0.499 | 0.502 | 0.547 | 0.203 | 0.380 | 0.758 | 0.332 |
rs2715150 | 0.416 | 0.042 | 0.687 | 0.432 | 0.556 | 0.556 | 0.339 |
rs550369696 | 0.001 | 0.000 | 0.000 | 0.000 | 0.000 | 0.062 | ND |
rs61741659 | 0.147 | 0.123 | 0.067 | 0.266 | 0.172 | 0.039 | 0.197 |
rs2877 | 0.781 | 0.694 | 0.993 | 0.684 | 0.920 | 0.984 | 0.684 |
rs762371134 | ND | ND | ND | ND | ND | 0.500 | 0.082 |
rs976714 | 0.389 | 0.103 | 0.440 | 0.361 | 0.399 | 0.453 | 0.305 |
rs10630259 | 0.994 | 1.000 | 0.996 | 0.987 | 0.991 | 1.000 | 0.993 |
rs2522833 | 0.416 | 0.042 | 0.687 | 0.432 | 0.556 | 0.565 | 0.339 |
rs10954696 | 0.389 | 0.102 | 0.442 | 0.361 | 0.399 | 0.431 | 0.305 |
rs10261848 | 0.019 | 0.213 | 0.000 | 0.000 | 0.008 | 0.009 | 0.037 |
rs76988622 | 0.004 | 0.032 | 0.000 | 0.000 | 0.000 | 0.000 | 0.014 |
rs28680905 | 0.013 | 0.179 | 0.000 | 0.000 | 0.000 | 0.000 | 0.034 |
rs182078347 | 0.013 | 0.000 | 0.000 | 0.000 | 0.000 | 0.000 | 0.003 |
rs6963292 | 0.020 | 0.279 | 0.000 | 0.000 | 0.008 | 0.000 | 0.048 |
rs377241009 | 0.000 | 0.000 | 0.000 | 0.000 | 0.000 | 0.000 | ND |
rs17148149 | 0.020 | 0.280 | 0.000 | 0.000 | 0.008 | 0.000 | 0.048 |
rs12668093 | 0.097 | 0.338 | 0.284 | 0.141 | 0.109 | 0.083 | 0.172 |
SNP ID | AMR | AFR | EAS | EUR | SAS | NAT | ABraOM |
---|---|---|---|---|---|---|---|
rs17156844 | 0.499 | 0.431 | 0.604 | 0.211 | 0.322 | 0.758 | 0.332 |
rs2715150 | 0.449 | 0.093 | 0.704 | 0.423 | 0.576 | 0.556 | 0.339 |
rs550369696 | 0.000 | 0.000 | 0.000 | 0.000 | 0.000 | 0.062 | ND |
rs61741659 | 0.129 | 0.138 | 0.053 | 0.235 | 0.192 | 0.039 | 0.197 |
rs2877 | 0.837 | 0.708 | 0.993 | 0.688 | 0.892 | 0.984 | 0.684 |
rs762371134 | 0.196 | 0.010 | 0.215 | 0.031 | 0.115 | 0.500 | 0.082 |
rs976714 | 0.412 | 0.127 | 0.497 | 0.359 | 0.391 | 0.453 | 0.305 |
rs10630259 | 0.995 | 0.998 | 1.000 | 0.982 | 0.987 | 1.000 | 0.993 |
rs2522833 | 0.453 | 0.096 | 0.706 | 0.426 | 0.582 | 0.565 | 0.339 |
rs10954696 | 0.411 | 0.126 | 0.499 | 0.359 | 0.392 | 0.431 | 0.305 |
rs10261848 | 0.009 | 0.205 | 0.000 | 0.000 | 0.008 | 0.009 | 0.037 |
rs76988622 | 0.009 | 0.031 | 0.000 | 0.000 | 0.000 | 0.000 | 0.014 |
rs28680905 | 0.007 | 0.174 | 0.000 | 0.000 | 0.000 | 0.000 | 0.034 |
rs182078347 | 0.009 | 0.000 | 0.000 | 0.000 | 0.000 | 0.000 | 0.003 |
rs6963292 | 0.009 | 0.255 | 0.000 | 0.000 | 0.008 | 0.000 | 0.048 |
rs377241009 | 0.000 | 0.000 | 0.000 | 0.000 | 0.000 | 0.000 | ND |
rs17148149 | 0.009 | 0.258 | 0.000 | 0.000 | 0.008 | 0.000 | 0.048 |
rs12668093 | 0.110 | 0.307 | 0.289 | 0.144 | 0.144 | 0.083 | 0.172 |
SNP ID | NAT vs. AMR | NAT vs. AFR | NAT vs. EAS | NAT vs. EUR | NAT vs. SAS | NAT vs. ABraOM |
---|---|---|---|---|---|---|
rs17156844 | 0.0060 | 0.0057 | 0.0689 | <0.0001 | <0.0001 | <0.0001 |
rs2715150 | 1 | <0.0001 | 1 | 1 | 1 | 0.0500 |
rs550369696 | 0.0488 | 0.0047 | 0.0133 | 0.0134 | 0.0148 | ND |
rs61741659 | 0.7027 | 1 | 1 | 0.0003 | 0.1424 | 0.0250 |
rs2877 | 0.0013 | 0.00012 | 1 | <0.0001 | 1 | <0.0001 |
rs762371134 | ND | ND | ND | ND | ND | ND |
rs976714 | 1 | <0.0001 | 1 | 1 | 1 | 1 |
rs10630259 | 1 | 1 | 1 | 1 | 1 | 1 |
rs2522833 | 1 | <0.0001 | 1 | 1 | 1 | 0.0500 |
rs10954696 | 1 | 1 | 1 | 1 | 1 | 1 |
rs10261848 | 1 | 0.0016 | 1 | 1 | 1 | 1 |
rs76988622 | 1 | 1 | 1 | 1 | 1 | 1 |
rs28680905 | 1 | 0.0008 | 1 | 1 | 1 | 1 |
rs182078347 | 1 | 1 | 1 | 1 | 1 | 1 |
rs6963292 | 1 | 1 | 1 | 1 | 1 | 1 |
rs377241009 | 1 | 1 | 1 | 1 | 1 | ND |
rs17148149 | 1 | <0.0001 | 1 | 1 | 1 | 1 |
rs12668093 | 1 | 0.0003 | 0.0195 | 1 | 1 | 1 |
SNP ID | NAT vs. AMR | NAT vs. AFR | NAT vs. EAS | NAT vs. EUR | NAT vs. SAS | NAT vs. ABraOM |
---|---|---|---|---|---|---|
rs17156844 | 0.0021 | 6.86 × 108 | 0.8747 | <0.0001 | 4.26 × 103 | 3.19 × 105 |
rs2715150 | 1 | 0.0001 | 1 | 1 | 1 | 0.05006 |
rs550369696 | 1.51 × 106 | 3.05 × 107 | 1.87 × 106 | 1.30 × 104 | 2.46 × 106 | ND |
rs61741659 | 1 | 0.8509 | 1 | 0.0010 | 0.02913 | 0.02507 |
rs2877 | 0.0232 | 1.18 × 108 | 1 | 1.75 × 104 | 1 | 3.26 × 107 |
rs762371134 | 4.83 × 108 | <0.0001 | 6.02 × 109 | <0.0001 | 4.02 × 102 | 1.32 × 101 |
rs976714 | 1 | 1.69 × 106 | 1 | 1 | 1 | 1 |
rs10630259 | 1 | 1 | 1 | 1 | 1 | 1 |
rs2522833 | 1 | <0.0001 | 1 | 1 | 1 | 0.0500 |
rs10954696 | 1 | 7.79 × 106 | 1 | 1 | 1 | 1 |
rs10261848 | 1 | 0.0012 | 0.62196 | 0.10114 | 1 | 1 |
rs76988622 | 1 | 1 | 1 | 1 | 1 | 1 |
rs28680905 | 1 | 0.0006 | 1 | 1 | 1 | 1 |
rs182078347 | 1 | 1 | 1 | 1 | 1 | 1 |
rs6963292 | 1 | 1.26 × 108 | 1 | 1 | 1 | 1 |
rs377241009 | 1 | 1 | 1 | 1 | 1 | ND |
rs17148149 | 1 | 6.99 × 107 | 1 | 1 | 1 | 1 |
rs12668093 | 1 | 0.0014 | 0.0064 | 1 | 1 | 1 |
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Cohen-Paes, A.d.N.; de Carvalho, D.C.; Pastana, L.F.; Dobbin, E.A.F.; Moreira, F.C.; de Souza, T.P.; Fernandes, M.R.; Leal, D.F.d.V.B.; de Sá, R.B.A.; de Alcântara, A.L.; et al. Characterization of PCLO Gene in Amazonian Native American Populations. Genes 2022, 13, 499. https://doi.org/10.3390/genes13030499
Cohen-Paes AdN, de Carvalho DC, Pastana LF, Dobbin EAF, Moreira FC, de Souza TP, Fernandes MR, Leal DFdVB, de Sá RBA, de Alcântara AL, et al. Characterization of PCLO Gene in Amazonian Native American Populations. Genes. 2022; 13(3):499. https://doi.org/10.3390/genes13030499
Chicago/Turabian StyleCohen-Paes, Amanda de Nazaré, Darlen Cardoso de Carvalho, Lucas Favacho Pastana, Elizabeth Ayres Fragoso Dobbin, Fabiano Cordeiro Moreira, Tatiane Piedade de Souza, Marianne Rodrigues Fernandes, Diana Feio da Veiga Borges Leal, Roberta Borges Andrade de Sá, Angélica Leite de Alcântara, and et al. 2022. "Characterization of PCLO Gene in Amazonian Native American Populations" Genes 13, no. 3: 499. https://doi.org/10.3390/genes13030499
APA StyleCohen-Paes, A. d. N., de Carvalho, D. C., Pastana, L. F., Dobbin, E. A. F., Moreira, F. C., de Souza, T. P., Fernandes, M. R., Leal, D. F. d. V. B., de Sá, R. B. A., de Alcântara, A. L., Guerreiro, J. F., Ribeiro-dos-Santos, Â., dos Santos, S. E. B., de Assumpção, P. P., & dos Santos, N. P. C. (2022). Characterization of PCLO Gene in Amazonian Native American Populations. Genes, 13(3), 499. https://doi.org/10.3390/genes13030499