La vitamina A: reguladora de la espermatogénesis
La vitamina A: reguladora de la espermatogénesis
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López LXR, Quiroga CFP. La vitamina A: reguladora de la espermatogénesis. Revista Investig. Salud Univ. Boyacá [Internet]. 30 de junio de 2015 [citado 22 de diciembre de 2024];2(1):63-79. Disponible en: https://revistasdigitales.uniboyaca.edu.co/index.php/rs/article/view/130
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La vitamina A es esencial para el desarrollo de las células germinales masculinas, la fertilidad y la espermatogénesis normal. El ácido retinoico, metabolito activo de la vitamina A, es necesario para la maduración de las espermatogonias y la entrada correcta de las células germinales en la profase meiótica en los testículos. La expresión de Stra8, fundamental en la meiosis y la espermatogénesis normal, está directamente relacionada con la disponibilidad del ácido retinoico.
Este artículo se centra en el proceso de espermatogénesis y la interacción de la vitamina A con el ciclo seminífero, a fin de explicar la relación existente entre la disminución de los aportes de vitamina A, y las alteraciones presentadas en la espermatogénesis de humanos y algunos animales. También, se consideran los efectos de otros genes implicados en la síntesis de la vitamina A, su transporte y su degradación, y se discuten los posibles mecanismos celulares que pueden verse afectados por la falta de señalización de la vitamina A, en particular, la regulación del ciclo celular y la interacción célula-célula, puntos críticos para la espermatogénesis normal.
En esta revisión de los 42 artículos científicos más relevantes del tema, se hizo una búsqueda de información en bases de datos como Science Direct, Scielo, Medline, Redalyc y Pubmed, durante los meses de enero a abril de 2014. Se encontró que en diversos estudios se ha demostrado que se puede controlar in vitro la proliferación de células germinales y su diferenciación, y además, que un deficiente consumo de vitamina A estaría relacionado con la disminución de la fertilidad masculina.
Palabras clave: vitamina A, espermatogénesis, bloqueadores de espermatogénesis, meiosis, ácido retinoico, testículos.
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1. Chung S, Wolgemuth D. Role of retinoid signaling in the regulation of spermatogenesis. Cytogenet Genome Res. (USA). 2004; 105(2-4):189-202.
2. Quintela L, Díaz C, Becerra J, Alonso G, Gracia S, Herradón P. Papel del β-caroteno y la vitamina A en la reproducción en el ganado vacuno: revisión. ITEA (Mex). 2008; 104(3): 399-410. 2008
3. Sharma RK, Agarwal A. Role of reactive oxygen species in male infertility. Urol. (USA). 1996; 48(6): 835-850.
4. Biesalski H, Schrezenmeir J, Weber P, Weiss H. Vitamine: Physiologie, pathophysiologie, therapie. En: Vitamin A and retinoids. 1 ed. USA: HE Book; 1997 3-19.
5. Rothman KJ, Moore LL, Singer MR, Nguyen U-SD, Mannino S, Milunsky A. Teratogenicity of high vitamin A intake. N Engl J Med. 1995; 333(21): 1369- 1373.
6. Semba RD. The role of vitamin A and related retinoids in immune function. Nutr Rev. 1998;56(1) 38-48.
7. Sasaki R. Pleiotropic functions of erythropoietin. Internal Med. 2003; 42(2): 142-149.
8. Nagao A. Absorption and function of dietary carotenoids. Forum Nutr. 2009;61(1): 55-63.
9. Livera G, Rouiller-Fabre V, Pairault C, Levacher C, Habert R. Regulation and perturbation of testicular functions by vitamin A. Reprod. . 2002;124(2):173- 80.
10. Vernet N, Dennefeld C, Rochette-Egly C, Oulad-Abdelghani M, Chambon P, Ghyselinck NB, et al. Retinoic acid metabolism and signaling pathways in the adult and developing mouse testis. Endocr. 2006;147(1): 96-110.
11. Hogarth CA, Griswold MD. The key role of vitamin A in spermatogenesis. J Clin Invest. 2010; 120(4): 956–962.
12. Toro AI. Espermograma. Med Lab. 2009;15(3-4): 145-69.
13. de Rooij DG. Proliferation and differentiation of spermatogonial stem cells. Reprod. 2001;121(3): 347-54.
14. Yoshida S, Sukeno M, Nakagawa T, Ohbo K, Nagamatsu G, Suda T, et al. The first round of mouse spermatogenesis is a distinctive program that lacks the self-renewing spermatogonia stage. Development. 2006;133(8): 1495-1505.
15. Tong M-H, Yang Q-E, Davis JC, Griswold MD. Retinol dehydrogenase 10 is indispensible for spermatogenesis in juvenile males. Proc Natl Acad Sci U S A. 2013;110(2): 543-8.
16. Rooij DG, Russell LD. All you wanted to know about spermatogonia but were afraid to ask. J Androl. 2000;21(6): 776-98.
17. Mark M, Jacobs H, Oulad-Abdelghani M, Dennefeld C, Féret B, Vernet N, et al. STRA8-deficient spermatocytes initiate, but fail to complete, meiosis and undergo premature chromosome condensation. J Cell Sci. 2008;121(19): 3233-3242.
18. Kerr J, Loveland K, O’Bryan M, de Kretser D. Cytology of the testis and intrinsic control mechanisms. En: Knobil and Neill’s Physiology of Reproduction. 1 Ed. Clayton: Elsevier Academic Press. 2006. 827-947.
19. Yan HH, Mruk DD, Cheng CY. Junction restructuring and spermatogenesis: The biology, regulation, and implication in male contraceptive development. Curr Top Dev Biol. 2007;80(1): 57-92.
20. Holdcraft RW, Braun RE. Androgen receptor function is required in Sertoli cells for the terminal differentiation of haploid spermatids. Development. 2004;131(2): 459-67.
21. França LR, Ogawa T, Avarbock MR, Brinster RL, Russell LD. Germ cell genotype controls cell cycle during spermatogenesis in the rat. Biol Reprod. 1998;59(6): 1371-1377.
22. Amann RP. The cycle of the seminiferous epithelium in humans: A need to revisit? J Androl. 2008;29(5): 469-487.
23. Clagett-Dame M, Knutson D. Vitamin A in reproduction and development. Nutrients. 2011;3(4): 385-428.
24. Hogarth CA, Amory JK, Griswold MD. Inhibiting vitamin A metabolism as an approach to male contraception. Trends Endocrinol Metab. 2011;22(4): 136-44.
25. Reproducción e inseminación artificial porcina [sede Web]*. Madrid: Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria; 1982. [acceso 19 de Marzo de 2013]. Martín-Rillo S.Disponible en: http:// agris.fao.org/agris-search/search. do?recordID=ES19830913155
26. Boticario C, Viña CA, Castro AP, Carchenilla MS, Velasco JA. Impacto de un complejo de antioxidantes sobre la fragmentación del ADN espermático en varones infértiles. Rev. int. androl. . 2010;8(3): 107-113.
27. Evenson DP, Larson KL, Jost LK. Sperm chromatin structure assay: Its clinical use for detecting sperm DNA fragmentation in male infertility and comparisons with other techniques. J Androl. 2002;23(1): 25-43.
28. Menon S, Rives N, Mousset-Siméon N, Sibert L, Vannier J, Mazurier S, et al. Fertility preservation in adolescent males: Experience over 22 years at Rouen University Hospital. Hum Reprod. 2009;24(1): 37-44.
29. Graves-Hoagland RL, Hoagland TA, Woody CO. Effect of β-carotene and vitamin A on progesterone production by bovine luteal cells. J Dairy Sci. 1988;71(4): 1058-1062.
30. Mason KE. Differences in testis injury and repair after vitamin A‐deficiency, vitamin E‐deficiency, and inanition. Am J Anat. 1933;52(2): 153-239.
31. Rhinn M, Dolle P. Retinoic acid signalling during development. Development. 2012;139(5): 843-58.
32. Doyle TJ, Braun KW, McLean DJ, Wright RW, Griswold MD, Kim KH. Potential functions of retinoic acid receptor A in Sertoli cells and germ cells during spermatogenesis. Ann N Y Acad Sci. 2007;1120(1): 114-130.
33. Anderson EL, Baltus AE, Roepers-Gajadien HL, Hassold TJ, de Rooij DG, Van Pelt AM, et al. Stra8 and its inducer, retinoic acid, regulate meiotic initiation in both spermatogenesis and oogenesis in mice. Proc Natl Acad Sci U S A. 2008;105(39): 14976-14980.
34. Griswold MD, Bishop PD, Kim KH, Ping R, Siiteri JE, Morales C. Function of vitamin A in normal and synchronized seminiferous tubulesa. Ann N Y Acad Sci. 1989;564(1): 154-172.
35. Zhou Q, Nie R, Li Y, Friel P, Mitchell D, Hess RA, et al. Expression of stimulated by retinoic acid gene 8 (Stra8) in spermatogenic cells induced by retinoic acid: An in vivo study in vitamin A-sufficient postnatal murine testes. Biol Reprod. 2008;79(1): 35-42.
36. Bowles J, Knight D, Smith C, Wilhelm D, Richman J, Mamiya S, et al. Retinoid signaling determines germ cell fate in mice. Science. 2006;312(5773): 596-600.
37. Koubova J, Menke DB, Zhou Q, Capel B, Griswold MD, Page DC. Retinoic acid regulates sex-specific timing of meiotic initiation in mice. Proc Natl Acad Sci U S A. 2006;103(8): 2474-2479.
38. Li H, Palczewski K, Baehr W, Clagett-Dame M. Vitamin A deficiency results in meiotic failure and accumulation of undifferentiated spermatogonia in prepubertal mouse testis. Biol Reprod. 2011;84(2): 336-341.
39. MacLean G, Li H, Metzger D, Chambon P, Petkovich M. Apoptotic extinction of germ cells in testes of Cyp26b1 knockout mice. Endocrinology. 2007;148(10): 4560-4567.
40. Baltus AE, Menke DB, Hu Y-C, Goodheart ML, Carpenter AE, de Rooij DG, et al. In germ cells of mouse embryonic ovaries, the decision to enter meiosis precedes premeiotic DNA replication. Nat Genet. 2006;38(12): 1430-1434.
41. Rossi P, Dolci S. Paracrine mechanisms involved in the control of early stages of mammalian spermatogenesis. Front Endocrinol. 2013;4(1): 181.
42. Appling DR, Chytil F. Evidence of a role for retinoic acid (vitamin A-acid) in the maintenance of testosterone production in male rats. Endocrinology. 1981;108(6): 2120-2123.
43. Marín-Guzmán J, Mahan D, Chung Y, Pate J, Pope W. Effects of dietary selenium and vitamin E on boar performance and tissue responses, semen quality, and subsequent fertilization rates in mature gilts. J Anim Sci. 1997;75(11): 2994-3003.
44. Martins S, Abrahão AAF, Vianna V, Andrade A, Arruda RAvaliação da suplementação de vitamina A nas características seminais em reprodutores suínos. Rev Bras de Zootecn. 2009;38(8):1518- 1524.
45. Aikawa H, Koyama S, Matsuda M, Nakahashi K, Akazome Y, Mori T. Relief effect of vitamin A on the decreased motility of sperm and the increased incidence of malformed sperm in mice exposed neonatally to bisphenol A. Cell Tissue Res. 2004;315(1): 119-124.
46. Abrahão AAF. Vitamina A na nutrição de cachaços: I-Fatores relacionados ao condicionamento de machos reprodutores suínos para a colheita de sêmen. II-Análise qualitativa e quantitativa do sêmen de cachaços submetidos à suplementação de vitamina A na dieta. [tesis doctoral]. São Paulo: Moretti, Anibal de Sant Anna (Catálogo USP), Universidade de São Paulo; 2006
47. Dohle GR. Male infertility in cancer patients: Review of the literature. Int Urol. 2010;17(4): 327-331. 48. Barazani Y, Katz BF, Nagler HM, Stember DS. Lifestyle, environment, and male reproductive health. Urol Clin North Am. 2014;41(1): 55-66.
49. Naumenko VA, Kushch AA. Herpes viruses and male infertility--is there any relationship?. Vopr Virusol. 2012;58(3): 4-9.
50. Keck C, Gerber-Schafer C, Clad A, Wilhelm C, Breckwoldt M. Seminal tract infections: Impact on male fertility and treatment options. Hum Reprod Update. 1998;4(6): 891-903.
2. Quintela L, Díaz C, Becerra J, Alonso G, Gracia S, Herradón P. Papel del β-caroteno y la vitamina A en la reproducción en el ganado vacuno: revisión. ITEA (Mex). 2008; 104(3): 399-410. 2008
3. Sharma RK, Agarwal A. Role of reactive oxygen species in male infertility. Urol. (USA). 1996; 48(6): 835-850.
4. Biesalski H, Schrezenmeir J, Weber P, Weiss H. Vitamine: Physiologie, pathophysiologie, therapie. En: Vitamin A and retinoids. 1 ed. USA: HE Book; 1997 3-19.
5. Rothman KJ, Moore LL, Singer MR, Nguyen U-SD, Mannino S, Milunsky A. Teratogenicity of high vitamin A intake. N Engl J Med. 1995; 333(21): 1369- 1373.
6. Semba RD. The role of vitamin A and related retinoids in immune function. Nutr Rev. 1998;56(1) 38-48.
7. Sasaki R. Pleiotropic functions of erythropoietin. Internal Med. 2003; 42(2): 142-149.
8. Nagao A. Absorption and function of dietary carotenoids. Forum Nutr. 2009;61(1): 55-63.
9. Livera G, Rouiller-Fabre V, Pairault C, Levacher C, Habert R. Regulation and perturbation of testicular functions by vitamin A. Reprod. . 2002;124(2):173- 80.
10. Vernet N, Dennefeld C, Rochette-Egly C, Oulad-Abdelghani M, Chambon P, Ghyselinck NB, et al. Retinoic acid metabolism and signaling pathways in the adult and developing mouse testis. Endocr. 2006;147(1): 96-110.
11. Hogarth CA, Griswold MD. The key role of vitamin A in spermatogenesis. J Clin Invest. 2010; 120(4): 956–962.
12. Toro AI. Espermograma. Med Lab. 2009;15(3-4): 145-69.
13. de Rooij DG. Proliferation and differentiation of spermatogonial stem cells. Reprod. 2001;121(3): 347-54.
14. Yoshida S, Sukeno M, Nakagawa T, Ohbo K, Nagamatsu G, Suda T, et al. The first round of mouse spermatogenesis is a distinctive program that lacks the self-renewing spermatogonia stage. Development. 2006;133(8): 1495-1505.
15. Tong M-H, Yang Q-E, Davis JC, Griswold MD. Retinol dehydrogenase 10 is indispensible for spermatogenesis in juvenile males. Proc Natl Acad Sci U S A. 2013;110(2): 543-8.
16. Rooij DG, Russell LD. All you wanted to know about spermatogonia but were afraid to ask. J Androl. 2000;21(6): 776-98.
17. Mark M, Jacobs H, Oulad-Abdelghani M, Dennefeld C, Féret B, Vernet N, et al. STRA8-deficient spermatocytes initiate, but fail to complete, meiosis and undergo premature chromosome condensation. J Cell Sci. 2008;121(19): 3233-3242.
18. Kerr J, Loveland K, O’Bryan M, de Kretser D. Cytology of the testis and intrinsic control mechanisms. En: Knobil and Neill’s Physiology of Reproduction. 1 Ed. Clayton: Elsevier Academic Press. 2006. 827-947.
19. Yan HH, Mruk DD, Cheng CY. Junction restructuring and spermatogenesis: The biology, regulation, and implication in male contraceptive development. Curr Top Dev Biol. 2007;80(1): 57-92.
20. Holdcraft RW, Braun RE. Androgen receptor function is required in Sertoli cells for the terminal differentiation of haploid spermatids. Development. 2004;131(2): 459-67.
21. França LR, Ogawa T, Avarbock MR, Brinster RL, Russell LD. Germ cell genotype controls cell cycle during spermatogenesis in the rat. Biol Reprod. 1998;59(6): 1371-1377.
22. Amann RP. The cycle of the seminiferous epithelium in humans: A need to revisit? J Androl. 2008;29(5): 469-487.
23. Clagett-Dame M, Knutson D. Vitamin A in reproduction and development. Nutrients. 2011;3(4): 385-428.
24. Hogarth CA, Amory JK, Griswold MD. Inhibiting vitamin A metabolism as an approach to male contraception. Trends Endocrinol Metab. 2011;22(4): 136-44.
25. Reproducción e inseminación artificial porcina [sede Web]*. Madrid: Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria; 1982. [acceso 19 de Marzo de 2013]. Martín-Rillo S.Disponible en: http:// agris.fao.org/agris-search/search. do?recordID=ES19830913155
26. Boticario C, Viña CA, Castro AP, Carchenilla MS, Velasco JA. Impacto de un complejo de antioxidantes sobre la fragmentación del ADN espermático en varones infértiles. Rev. int. androl. . 2010;8(3): 107-113.
27. Evenson DP, Larson KL, Jost LK. Sperm chromatin structure assay: Its clinical use for detecting sperm DNA fragmentation in male infertility and comparisons with other techniques. J Androl. 2002;23(1): 25-43.
28. Menon S, Rives N, Mousset-Siméon N, Sibert L, Vannier J, Mazurier S, et al. Fertility preservation in adolescent males: Experience over 22 years at Rouen University Hospital. Hum Reprod. 2009;24(1): 37-44.
29. Graves-Hoagland RL, Hoagland TA, Woody CO. Effect of β-carotene and vitamin A on progesterone production by bovine luteal cells. J Dairy Sci. 1988;71(4): 1058-1062.
30. Mason KE. Differences in testis injury and repair after vitamin A‐deficiency, vitamin E‐deficiency, and inanition. Am J Anat. 1933;52(2): 153-239.
31. Rhinn M, Dolle P. Retinoic acid signalling during development. Development. 2012;139(5): 843-58.
32. Doyle TJ, Braun KW, McLean DJ, Wright RW, Griswold MD, Kim KH. Potential functions of retinoic acid receptor A in Sertoli cells and germ cells during spermatogenesis. Ann N Y Acad Sci. 2007;1120(1): 114-130.
33. Anderson EL, Baltus AE, Roepers-Gajadien HL, Hassold TJ, de Rooij DG, Van Pelt AM, et al. Stra8 and its inducer, retinoic acid, regulate meiotic initiation in both spermatogenesis and oogenesis in mice. Proc Natl Acad Sci U S A. 2008;105(39): 14976-14980.
34. Griswold MD, Bishop PD, Kim KH, Ping R, Siiteri JE, Morales C. Function of vitamin A in normal and synchronized seminiferous tubulesa. Ann N Y Acad Sci. 1989;564(1): 154-172.
35. Zhou Q, Nie R, Li Y, Friel P, Mitchell D, Hess RA, et al. Expression of stimulated by retinoic acid gene 8 (Stra8) in spermatogenic cells induced by retinoic acid: An in vivo study in vitamin A-sufficient postnatal murine testes. Biol Reprod. 2008;79(1): 35-42.
36. Bowles J, Knight D, Smith C, Wilhelm D, Richman J, Mamiya S, et al. Retinoid signaling determines germ cell fate in mice. Science. 2006;312(5773): 596-600.
37. Koubova J, Menke DB, Zhou Q, Capel B, Griswold MD, Page DC. Retinoic acid regulates sex-specific timing of meiotic initiation in mice. Proc Natl Acad Sci U S A. 2006;103(8): 2474-2479.
38. Li H, Palczewski K, Baehr W, Clagett-Dame M. Vitamin A deficiency results in meiotic failure and accumulation of undifferentiated spermatogonia in prepubertal mouse testis. Biol Reprod. 2011;84(2): 336-341.
39. MacLean G, Li H, Metzger D, Chambon P, Petkovich M. Apoptotic extinction of germ cells in testes of Cyp26b1 knockout mice. Endocrinology. 2007;148(10): 4560-4567.
40. Baltus AE, Menke DB, Hu Y-C, Goodheart ML, Carpenter AE, de Rooij DG, et al. In germ cells of mouse embryonic ovaries, the decision to enter meiosis precedes premeiotic DNA replication. Nat Genet. 2006;38(12): 1430-1434.
41. Rossi P, Dolci S. Paracrine mechanisms involved in the control of early stages of mammalian spermatogenesis. Front Endocrinol. 2013;4(1): 181.
42. Appling DR, Chytil F. Evidence of a role for retinoic acid (vitamin A-acid) in the maintenance of testosterone production in male rats. Endocrinology. 1981;108(6): 2120-2123.
43. Marín-Guzmán J, Mahan D, Chung Y, Pate J, Pope W. Effects of dietary selenium and vitamin E on boar performance and tissue responses, semen quality, and subsequent fertilization rates in mature gilts. J Anim Sci. 1997;75(11): 2994-3003.
44. Martins S, Abrahão AAF, Vianna V, Andrade A, Arruda RAvaliação da suplementação de vitamina A nas características seminais em reprodutores suínos. Rev Bras de Zootecn. 2009;38(8):1518- 1524.
45. Aikawa H, Koyama S, Matsuda M, Nakahashi K, Akazome Y, Mori T. Relief effect of vitamin A on the decreased motility of sperm and the increased incidence of malformed sperm in mice exposed neonatally to bisphenol A. Cell Tissue Res. 2004;315(1): 119-124.
46. Abrahão AAF. Vitamina A na nutrição de cachaços: I-Fatores relacionados ao condicionamento de machos reprodutores suínos para a colheita de sêmen. II-Análise qualitativa e quantitativa do sêmen de cachaços submetidos à suplementação de vitamina A na dieta. [tesis doctoral]. São Paulo: Moretti, Anibal de Sant Anna (Catálogo USP), Universidade de São Paulo; 2006
47. Dohle GR. Male infertility in cancer patients: Review of the literature. Int Urol. 2010;17(4): 327-331. 48. Barazani Y, Katz BF, Nagler HM, Stember DS. Lifestyle, environment, and male reproductive health. Urol Clin North Am. 2014;41(1): 55-66.
49. Naumenko VA, Kushch AA. Herpes viruses and male infertility--is there any relationship?. Vopr Virusol. 2012;58(3): 4-9.
50. Keck C, Gerber-Schafer C, Clad A, Wilhelm C, Breckwoldt M. Seminal tract infections: Impact on male fertility and treatment options. Hum Reprod Update. 1998;4(6): 891-903.
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