ASM  Vol.3 No.3 A , August 2013
Testosterone Levels and Development of the Penile Spines and Testicular Tissue during the Postnatal Growth in Wistar Rats
Aim of Study: Gonadal hormones exert a profound influence on the development, structure and function of the sexual organs. The testosterone is one of the androgens that plays an essential role in the development of sexual organs in male mammals. Therefore, the present study was undertaken to evaluate the testosterone levels and developmental pattern of the penile spines and seminiferous tubules during early postnatal life of Wistar rats. Methods and Materials: At 7, 14, 21, 28, 35, 42, 49, 56, 63 and 70 days after birth, penile and testicular tissues of male rats were dissected out and fixed for histological study and plasma testosterone levels were determined using high resolution chromatography. Results: An increase in the number of penile follicles, primarily in the distal region of the penis, was observed from postnatal days 14 to 42, followed by a gradual decrease. Penile spines were absent from birth until the first growth peak, which was observed at 42 postnatal days. Both testicular weight and the area of seminiferous tubules showed gradual increases before achieving their highest values at 42 postnatal days. Similarly, a gradual increase in testosterone levels was detected from day 28, with a peak at 42 postnatal days. Conclusions: These data show a temporal association between the development of the penile spines and testicular tissue with gradual increases in testosterone levels. These results may contribute to a better understanding of the behavioral, hormonal and morphological changes underlying sexual maturation in male rats.

Cite this paper
M. Silva, R. Villaseñor, S. Márquez, M. González, H. Jaime, X. García and J. Montiel, "Testosterone Levels and Development of the Penile Spines and Testicular Tissue during the Postnatal Growth in Wistar Rats," Advances in Sexual Medicine, Vol. 3 No. 3, 2013, pp. 1-9. doi: 10.4236/asm.2013.33A001.

[1]   F. W. George and J. D. Wilson, “Sex Determination and Differentiation,” In: E. Knobil and J. Neil, Eds., Physiology of Reproduction, 2nd Edition, Raven Press, New York, 1994, pp. 3-28.

[2]   R. S. Ge, L. X. Shan and M. P. Hardy, “Pubertal Development of Leydig Cells,” In: D. Lussell, Ed., The Leydig Cell, River Press, Vienna, 1996, pp. 159-173.

[3]   R. S. Ge, Q. Dong, C. M. Sottas, H. Chen, B. R. Zirkin and M. P. Hardy, “Gene Expression in Rat Leydig Cells during Development from the Progenitor to Adult Stage: A Cluster Analysis,” Biology of Reproduction, Vol. 72, No. 6, 2005, pp. 1405-1415. doi:10.1095/biolreprod.104.037499

[4]   P. S. Vilamaior, S. R. Taboga and H. F. Carvalho, “Postnatal Growth of the Ventral Prostate in Wistar Rats: A Stereological and Morphometrical Study,” The Anatomical Record Part A: Discoveries and Molecular, Cellular, and Evolution Biology, Vol. 288A, No. 8, 2006, pp. 885-892. doi:10.1002/ar.a.20363

[5]   M. Dorostghoal, F. Sorooshnia and A. Zardkaf, “Stereological Analysis of Wistar Rat Testis during Early Post-Natal Development,” Anatomia, Histologia Embryologia, Vol. 40, No. 2, 2011, pp. 89-94. doi:10.1111/j.1439-0264.2010.01043.x

[6]   C. A. Anderson and R. L. Clark, “External Genitalia of the Rat: Normal Development and the Histogenesis of 5a-Reductase Inhibitor-Induced Abnormalities,” Teratology, Vol. 42, No. 5, 1990, pp. 483-496. doi:10.1002/tera.1420420505

[7]   C. A. Wilson and D. C. Davies, “The Control of Sexual Differentiation of the Reproductive System and Brain,” Reproduction, Vol. 133, No. 2, 2007, pp. 331-359. doi:10.1530/REP-06-0078

[8]   C. C. Korenbrot, I. T. Huhtaniemi and R. I. Weiner, “Preputial Separation as an External Sign of Pubertal Development in the Male Rat,” Biology of Reproduction, Vol. 17, No. 2, 1977, pp. 298-303. doi:10.1095/biolreprod17.2.298

[9]   B. D. Sachs and R. L. Meisel, “Pubertal Development of Penile Reflexes and Copulation in Male Rats,” Psychoneuroendocrinology, Vol. 4, No. 4, 1979, pp. 287-296. doi:10.1016/0306-4530(79)90013-1

[10]   L. O′Donnell, R. I. McLachlan, N. G. Wreford and D. M. Robertson, “Testosterone Promotes the Conversion of Round Spermatids between Stages Vll-Vlll of the Rat Spermatogenic Cycle,” Endocrinology, Vol. 135, No. 6, 1994, pp. 2608-2614. doi:10.1210/en.135.6.2608

[11]   N. Sofikitis, K. Ono, Y. Yamamoto, H. Papadopoulosand and I. Miyagawa, “Influence of the Male Reproductive Tract on the Reproductive Potential of Round Spermatids Abnormally Released from the Seminiferous Epithelium,” Human Reproduction, Vol. 14, No. 8, 1999, pp. 1998-2006. doi:10.1093/humrep/14.8.1998

[12]   M. Welsh, R. M. Sharpe, M. Walker, L. B. Smith and P. T. Saunders, “New Insights into the Role of Androgens in Wolffian Duct Stabilization in Male and Female Rodents,” Endocrinology, Vol. 150, No. 5, 2009, pp. 2472-2480. doi:10.1210/en.2008-0529

[13]   M, Arteaga Silva, R. M. Vigueras Villasenor, S. Retana Márquez, M. Hernández González, C. Chihuahua Serrano, H, Bonilla-Jaime, J. L. Contreras and G. Moralí, “Testosterone, Androstenedione, and 5alpha-Dihydrotestosterone on Male Sexual Behavior and Penile Spines in the Hamster,” Journal Physiology and Behavior, Vol. 94, No. 3, 2008, pp. 412-421.

[14]   H. Kanagawa and E. S. Hafez, “The Penis,” In: E. S. Hafez, Ed., Scanning Electron Microscopic Atlas of Mammalian Reproduction, Thieme, Stuttgart, 1975.

[15]   G. T. Taylor, D, Komitowski and J. Weiss, “Light and Scanning Electron Microscopic Study of Testosterone-Restored Penile Papillae in Castrated Rats,” Journal Anatomical Records, Vol. 205, No. 3, 1983, pp. 277-286. doi:10.1002/ar.1092050305

[16]   G.T. Taylor, J. Weissand and D. Komitowski, “Reproductive Physiology and Penile Papillae Morphology of Rats after Sexual Experience,” Journal of Endocrinology, Vol. 98, No. 3, 1983, pp. 155-163. doi:10.1677/joe.0.0980155

[17]   B. D. Sachs, G. B. Glater and J. K. O’Hanlon, “Morphology of the Erect Glans Penis in Rats under Various Gonadal Hormone Conditions,” The Anatomical Records, Vol. 210, No. 1, 1984, pp. 45-52. doi:10.1002/ar.1092100108

[18]   R. Murakami. “A Histological Study of the Development of the Penis of Wild-Type and Androgen-Insensitive Mice,” Journal of Anatonomy, Vol. 153, 1987, pp. 223-231.

[19]   B. D. Sachs, “Role of Striated Penile Muscles in Penile Reflexes, Copulation, and Induction of Pregnancy in the Rat,” Journal of Reproduction and Fertility, Vol. 66, No. 2, 1982, pp. 433-443. doi:10.1530/jrf.0.0660433

[20]   J. K. O’Hanlonand and B. D. Sachs, “Fertility of Mating in Rats (Rattusnorvegicus): Contributions of Androgen-Dependent Morphology and Actions of the Penis,” Journal of Comparative Psychology, Vol. 100, No. 2, 1986, pp. 178-187. doi:10.1037/0735-7036.100.2.178

[21]   N. C. Kierniesky and A. A. Gerall, “Effects of Testosterone Propionate Implants in the Brain on the Sexual Behavior and Peripheral Tissue of the Male Rat,” Journal Physiology and Behavior, Vol. 11, No. 5, 1973, pp. 633-640. doi:10.1016/0031-9384(73)90248-5

[22]   M. J. Baum, S. A. Tobet, M. S. Starr and W. G. Bradshaw, “Implantation of Dihydrotestosterone Propionate into the Lateral Septum or Medial Amygdale Facilitates Copulation in Castrated Mate Rats Given Estradiol Systemically,” Hormones and Behavior, Vol. 16, No. 2, 1982, pp. 208-223. doi:10.1016/0018-506X(82)90020-4

[23]   C. H. Phoenix, K. H. Copenhaver and R. M. Brenner, “Scanning Electron Microscopy of Penile Papillae in Intact and Castrated Rats,” Hormones and Behavior, Vol. 7, No. 2, 1976, pp. 217-227. doi:10.1016/0018-506X(76)90049-0

[24]   F. A. Beach and L. P. Nucci, “Long-Term Effects of Testosterone Phenyl Acetate on Sexual Morphology and Behavior in Castrated Male Rats,” Hormones and Behavior, Vol. 1, No. 1, 1970, pp. 223-234. doi:10.1016/0018-506X(70)90016-4

[25]   H. H. Feder, “The Comparative Actions of Testosterone and 5α-Androstan-17β-ol-3-One Propionate on the Reproductive Behavior, Physiology, and Morphology of Male Rats,” The Journal of Endocrinology, Vol. 51, No. 2, 1971, pp. 241-252. doi:10.1677/joe.0.0510241

[26]   D. M. Kretser and J. B. Kerr. “The Cytology of the Testis,” In: E. Knobil and J. Neil, Eds., Physiology of Reproduction, 2nd Edition, Raven Press, New York, 1994, pp. 1177-1290.

[27]   R. D. Johnson and Z. Halata, “Topography and Ultrastructure of Sensory Nerve Endings in the Glans Penis of the Rat,” The Journal of Comparative Neurology, Vol. 312, No. 2, 1991, pp. 299-310. doi:10.1002/cne.903120212

[28]   H. Mori and A. K. Christensen, “Morphometric Analysis of Leydig Cells in the Normal Rat Testis,” Journal of Cell Biology, Vol. 84. No. 2, 1982, pp. 340-354. doi:10.1083/jcb.84.2.340

[29]   T. Y. Wing and A. K. Christensen, “Morphometric Studies on Rat Seminiferous Tubules,” Annals Journal of Anatomy, Vol. 165, No. 1, 1982, pp. 13-25.

[30]   F. Gaytan, M. Concepcion, L. E. Mu?oz and R. Paniagua, “Morphometric Aspects of Rat Testis Development,” Journal of Anatomy, Vol. 145, 1996, pp. 155-159.

[31]   Y. N. Zhengwei, G. Wreford and D. M. de Kretser, “A Quantitative Study of Spermatogenesis in the Developing Rat Testis,” Biology of Reproduction, Vol. 43, No. 4, 1990, pp. 629-635. doi:10.1095/biolreprod43.4.629

[32]   I. S. Kim and H. H. Yang, “Morphometric Study of the Testicular Interstitium of the Rat during Postnatal Development,” Korean Journal Anatomy, Vol. 32, No. 6, 1999, pp. 849-858.

[33]   C. Woodward and P. Emery, “Determination of Plasma Corticosterone Using High Performance Liquid Chromatography,” Journal of Chromatography, Vol. 419, 1987, pp. 280-284.

[34]   W. E. Berndtson, “Methods for Quantifying Mammalian Spermatogenesis: A Review,” Journal of Animal Science, Vol. 44, No. 5, 1977, pp. 818-833.

[35]   H. Bonilla-Jaime, G. Vázquez-Palacios, M. Arteaga-Silva and S. Retana-Márquez, “Hormonal Responses to Different Sexually Related Conditions in Male Rats,” Hormones and Behavior, Vol. 49, No. 3, 2006, pp. 376-382. doi:10.1016/j.yhbeh.2005.08.005

[36]   C. L. Moore and S. A. Rogers, “Contribution of Self-Grooming to the Onset of Puberty in Male Rats,” Developmental Psychobiology, Vol. 17, No. 3, 1984, pp. 243-253.

[37]   C. P. Stone, “The Awakening of Copulatory Ability in the Male Albino Rat,” American Journal of Physiology, Vol. 68, 1924, pp. 407-424.

[38]   M. Hernández-González, “Prepubertal Genital Grooming and Penile Erections in Relation to the Sexual Behavior of Rats,” Journal Physiology and Behavior, Vol. 71, No. 1-2, 2000, pp. 51-56. doi:10.1016/S0031-9384(00)00320-6

[39]   M. Hernández-González, K. E. Sánchez, M. V. Blando, S. Orozco-Suarez, M. Arteaga-Silva and M. A. Guevara, “Effects of Alcohol on Behavioral and Morphologic Indices of Sexual Maturation in Male Rats,” Alcohol, Vol. 33, No. 2, 2004, pp. 117-126. doi:10.1016/j.alcohol.2004.06.002

[40]   C. L. Moore, “Sex Differences in Self-Grooming of Rats: Effects of Gonadal Hormones and Context,” Journal Physiology and Behavior, Vol. 36, No, 3, 1986, pp. 451-455. doi:10.1016/0031-9384(86)90314-8

[41]   M. N. Simmons and J. S. Jones, “Male Genital Morphology and Function: An Evolutionary Perspective,” The Journal of Urology, Vol. 177, No. 5, 2007, pp. 1625-1631. doi:10.1016/j.juro.2007.01.011

[42]   D. S. Johnston, L. D. Russell, P. J. Friel and M. D. Griswold, “Murine Germ Cells Do Not Require Functional Androgen Receptors to Complete Spermatogenesis Following Spermatogonial Stem Cell Transplantation,” Endocrinology, Vol. 142, No. 6, 2001, pp. 2405-2408. doi:10.1210/en.142.6.2405

[43]   J. D. Wilson. “Metabolism of Testicular Androgens,” In: D. W. Hamilton and R. O. Greep, Eds., Handbook of Physiology, Williams and Wilkins Co., Baltimore, 1975, pp. 143-172.

[44]   H. E. MacLean, W. S. Chiu, A.J. Notini, A. M. Axell, R. A. Davey, J. F. McManus, C. Ma, D. R. Plant, G. S. Lynch and J. D. Zajac, “Impaired Skeletal Muscle Development and Function in Male, But Not Female, Genomic Androgen Receptor Knockout Mice,” FASEB Journal: Official Publication of the Federation of American Societies for Experimental Biology, Vol. 22, No. 8, 2008, pp. 2676-2689.

[45]   Ophoff, K. Van Proeyen, F. Callewaert, K. De Gendt, K. De Bock, A. Vanden Bosch, G. Verhoeven, P. Hespel, and D. Vanderschueren, “Androgen Signaling in Myocytes Contributes to the Maintenance of Muscle Mass and Fiber Type Regulation But Not to Muscle Strength or Fatigue,” Endocrinology, Vol. 150, No. 8, 2009, pp. 3558-3566. doi:10.1210/en.2008-1509

[46]   D. K. Lee, “Androgen Receptor Enhances Myogenin Expression and Accelerates Differentiation,” Biochemical and Biophysical Research Communications, Vol. 294, No. 2, 2002, pp. 408-413. doi:10.1016/S0006-291X(02)00504-1

[47]   Y. Joubert, C. Tobin and M. C. Lebart, “Testosterone-Induced Masculinization of the Rat Levator Ani Muscle during Puberty,” Developmental Biology, Vol. 162, No. 1, 1994, pp. 104-110. doi:10.1006/dbio.1994.1070

[48]   P. Diel, D. Baadners, K. Schlüpmann, M. Velders and J. P. Schwarz, “C2C12 myoblastoma Cell Differentiation and Proliferation Is Stimulated by Androgens and Associated with a Modulation of Myostatin and Pax7 Expression,” Journal of Moecularl Endocrinology, Vol. 40, No. 5, 2008, pp. 231-241. doi:10.1677/JME-07-0175

[49]   K. De Gendt and G. Verhoeven, “Tissue-and Cell-Specific Functions of the Androgen Receptor Revealed through Conditional Knockout Models in Mice,” Molecular and Cellular Endocrinology, Vol. 352, No. 1-2, 2012, pp. 13-25. doi:10.1016/j.mce.2011.08.008