Pituitary cells in man during aging: an immunohistological and morphometric study
Keywords:
ACTH cells, GH cells, LH cells, FS cells, aging
Abstract
Background: Aging is a multifactorial process, which inevitably leads to numerous changes in the life of each individual. As the lifespan of people around the world has increased, scientists began to study the mechanisms that would enable high quality and safe aging. The aim of the investigation was to indicate the changes in the cells of the pituitary gland caused by the aging process.
Methods: In order to write this review, we undertook an electronic literature search through the PubMed and Google Scholar databases with the terms aging, histological, ultrastructure of pituitary cells, using also the "related articles" option, as well as an additional analysis of authored and co-authored articles, which were necessary for this type of publication.
Results: This review article describes the immunohistological, ultrastructural and morphometric characteristics of adrenocorticotropic (ACTH), somatotropic (GH), gonadotropic (LH) and folliculostellate (FS) pituitary cells during aging, in young (about 47 years) and old (over 70 years) cadavers.
Conclusions: The described immunohistological and morphometric characteristics of the pituitary cells in this review indicated a significant increase in the volume density of ACTH, GH and LH cells in old cadavers, which suggested an attempt of these cells to bring the pituitary gland to a relatively balanced state.
References
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11. van der Spoel E, Roelfsema F, van Heemst D. Relationships between 24-hours LH and testosterone concentrations and with other pituitary hormones in healthy older men. Journal of the Endocrine Society 2021; 5(9):1–15. DOI:10.1210/jendso/bvab075
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16. Keenan DM, Hefti JP, Veldhuis JD, Von Wolff M. Regulation and adaptation of endocrine axes at high altitude. Am J Physiol Endocrinol Metab. 2020 318(2):297–309. DOI:10.1152/ajpendo.00243.2019
17. Jovanović I, Ugrenović S, Ljubomirović M, Vasović LJ, Cukuranović R, Stefanović V. Folliculo-stellate cells - potential mediators of the inflammaging-induced hyperactivity of the hypothalamic-pituitary-adrenal axis in healthy elderly individuals. Med Hypotheses 2014; 83(4):501–5. DOI:10.1016/j.mehy.2014.08.018
18. Čukuranović-Kokoris J, Jovanović I, Pantović V, Krstić M, Stanojković M, Milošević V, et al; Morphometric analysis of the folliculostellate cells and luteinizing hormone gonadotropic cells of the anterior pituitary of the men during the aging process. Tissue and Cell 2017; 49(1): 78–85. DOI:10.1016/j.tice.2016.11.006
19. Ajdžanović V, Trifunović S, Miljić D, Šošić-Jurjević B, Filipović B, Miler M, et al: Somatopause, weaknesses of the therapeutic approaches and the cautious optimism based on experimental ageing studies with soy isoflavones. EXCLI Journal 2018; 17:279–301. DOI:10.17179/excli2017-956
20. Kelberman D, Rizzoti K, Lovell-Badge R, Robinson IC, Dattani MT. Genetic regulation of pituitary gland development in human and mouse. Endocr Rev 2009; 30 (7):790–829. DOI:10.1210/er.2009-0008
21. Baisre de León A. Histopathology of the pituitary lesions. Otolaryngol Clin North Am. 2022; 55(2):265–85. DOI:10.1016/j.otc.2021.12.003
22. Rudman D, Kutner M H, Rogers C M, Lubin M F, Fleming G A, Bain R P. Impaired growth hormone secretion in the adult population: relation to age and adiposity. J Clin Invest. 1981;67(5):1361–9. DOI:10.1172/jci110164
23. Sattler FR. Growth hormone in the aging male. Best Pract Res Clin Endocrinol Metab 2013; 27(4):541–55. DOI:10.1016/j.beem.2013.05.003
24. Adamo ML, Farrar RP. Resistance training, and IGF involvement in the maintenance of muscle mass during the aging process. Ageing Res Rev 2006;5(3):310–31. DOI:10.1016/j.arr.2006.05.001
25. Demiral M, Karaca MS , Unal E, Baysal B, Baran R, Demirbilek H, et al; A novel diagnostic tool for the evaluation of hypothalamic-pituitary region and diagnosis of growth hormone deficiency: pons ratio. J Pediatr Endocrinol Metab. 2020; 33(6):735–42. DOI:10.1515/jpem-2019-0321
26. Milošević V, Brkić B, Velkovski S, Sekulić M, Lovren M, Starčević V, et al; Morphometric and Functional changes of rat pituitary somatotropes and lactotropes after central administration of somatostatin. Pharmacology 1998; 57(1):28–34. DOI:10.1159/000028223
27. Veldhuis JD. Aging and hormones of the hypothalamo-pituitary axis: gonadotropic axis in men and somatotropic axes in men and women. Ageing Res Rev 2008; 7(3):189–208. DOI:10.1016/j.arr.2007.12.005
28. Perrini S, Laviola L, Carreira MC, Cignarelli A, Natalicchio A, Giorgino F. The GH/IGF1 axis and signaling pathways in the muscle and bone: mechanisms underlying age-related skeletal muscle wasting and osteoporosis. J Endocrinol 2010; 205(3):201–10. DOI:10.1677/JOE-09-0431
29. Antić VM, Stefanović N, Jovanović I, Antić M, Milić M, Krstić M, et al;. Morphometric analysis of somatotropic cells of the adenohypophysis and muscle fibers of the psoas muscle in the process of aging in humans. Ann Anat 2015; 200:44–53. DOI:10.1016/j.aanat.2015.01.006
30. Pamphlett R, Jew SK, Doble PA, Bishop DP. Elemental analysis of aging human pituitary glands implicates mercury as a contributor to the somatopause. Front Endocrinol (Lausanne). 2019;10:419. DOI:10.3389/fendo.2019.00419
31. Veldhuis JD. Changes in pituitary function with ageing and implications for patient care. Nat Rev Endocrinol. 2013;9(4):205–15. DOI:10.1038/nrendo.2013.38
32. Childs GV. Cytochemical studies of multifunctional gonadotropes. Microsc Res Tech 1997;39 (2):114e130. DOI:10.1002/(SICI)1097-0029(19971015)39:2
33. Grumbach MM, A window of opportunity: The diagnosis of gonadotropin deficiency in the male infant, J Clin Endocrinol Metab 2005;90(5):3122–7. DOI:10.1210/jc.2004-2465
34. Seminara SB, Hayes FJ, Crowley WF Jr. Gonadotropin releasing hormone deficiency in the human (idiopathic hypogonadotropic hypogonadism and Kallmann’s syndrome): Pathophysiological and genetic considerations. Endocr Rev 1998;19(5):521–39. DOI:10.1210/edrv.19.5.0344
35. Uwaifo GI. The Human Hypothalamus. Contemporary Endocrinology 2021; pp.1–528. DOI:10.1007/978-3-030-62187-2
36. Brioude F, Bouligand J, Trabado S., Francou B, Salenave S, Kamenicky P, et al; Non-syndromic congenital hypogonadotropic hypogonadism: Clinical presentation and genotypephenotype relationships. Eur J Endocrinol 2010; 162(5):835–51. DOI:10.1530/EJE-10-0083
37. Grumbach M.M. The neuroendocrinology of human puberty revisited. Horm Res 2002;57 (Suppl 2):2–14. DOI:10.1159/000058094
38. Bhasin S, Calof OM., Storer TW, Lee ML, Mazer NA, Jasuja R, et al:. Drug insight: Testosterone and selective androgen receptor modulators as anabolic therapies for chronic illness and aging. Nat Clin Pract Endocrinol Metab 2006; 2(3):146–59. DOI:10.1038/ncpendmet0120
39. Kaiser U. B. Gonadotropin Hormones. The Pituitary 2011; pp. 205–260. DOI:10.1016/b978-0-12-380926-1.10007-0
40. Roelfsema F, Liu PY, Takahashy PY, Yang RJ, Veldhuis JD. Dynamic interactions betwen LH and testosterone in healthy community-dwelling men: impact of age and body composition. J Clin Endocrinol Metab 2020; 105(3):628–41. DOI:10.1210/clinem/dgz246
41. Herman-Bonert VS, Melmed S. Growth Hormone. The Pituitary 2011;83–117. DOI:10.1016/b978-0-12-380926-1
42. Dudek P, Kozakowski J, Zgliczynski W. Late-onset hypogonadism. Menopause Rev 2017;16(2): 66–9. DOI:10.5114/pm.2017.68595
43. Veldhuis JD, Keenan D, Iranmanesh A, Takahashi P, Nehra A. The Ensemble Male Hypothalamo-Pituitary-Gonadal Axis. In: Timiras PS, editor. Physiological Basis of Aging and Geriatrics. 4th ed. CRC Press 2007; pp. 185–203. DOI:10.3109/9781420007091-14
44. Perez-Castro C, Renner U, Haedo MR, Stalla GK, Arzt E. Cellular and molecular specificity of pituitary gland physiology. Physiol Rev 2012; 92(1):1–38. DOI:10.1152/physrev.00003.2011
45. Nestorović N, Ristić N, Ajdžanović V, Trifunović S, Milošević V. Morphological and functional changes of pituitary GH and PRL cells following prolonged exposure of female rats to constant light. Experimental and Applied Biomedical Research 2023; 24(3):219–25. DOI:10.2478/sjecr-2019-0063
46. Takashi S. Heterogeneity and development of somatotropes and mammotropes in the rat. Zool Sci 1992;9:901–24.
47. Kurosumi K. Ultrastructural immunocytochemistry of the adenohypophysis in the rat: a review. J Electron Microsc Tech 1991;19(1): 42–56. DOI:10.1002/jemt.1060190105
48. Čukuranović-Kokoris J, Marković Filipović J, Đorđević M, Kundalić B, Stojanović V, Trandafilović M, Graovac I, Milošević V, Čukuranović R. Correlation analysis of pituitary lutheinizing and somatotropic cells in man during aging. Acta medica Medianae 2024; 63(1):90–6. DOI:10.5633/amm.2024.0110
49. Horvath E, Kovacs K. Ultrastructural diagnosis of human pituitary adenomas. Microsc Res Tech 1992; 20(2):107–35. DOI:10.1002/jemt.1070200202
2. Dorton A M. The pituitary gland: embryology, physiology, and pathophysiology. Neonatal Netw. 2000;19(2):9–17. DOI:10.1891/0730-0832.19.2.9
3. Sheng JA, Bales NJ, Myers SA, Bautista AI, Roueinfar M, Hale TM, et al; The Hypothalamic-Pituitary-Adrenal Axis: Development, programming actions of hormones, and maternal-fetal interactions. Front Behav Neurosci. 2021;14:601939. DOI:10.3389/fnbeh.2020.601939
4. Inoue K, Couch EF, Takano K, Ogawa S. The structure and function of folliculo-stellate cells in the anterior pituitary gland. Arch Histol Cytol 1999; 62(3):205–18. DOI:1679/aohc.62.205
5. Milošević V, Nestorović N, Negić N, Filipović B, Brkić B, Starčević V. Characteristics of the pituitary immunopositive ACTH cells. In rat females after chronic exposure to constant light. Jugosl Med Biohem. 2003; 22(1):27–32. DOI:10.2298/JMH0301027M
6. Lačković V, Bumbaširević V. Histological atlas 6th edition, Data Status, 2021; pp.1–363. ISBN:9788674787236
7. Bahraman AG, Jamshidzadeh A, Keshavarzi M, Arabnezhad M-R, Mohammadi H, Mohammadi-Bardbori A. α-Melanocyte-stimulating hormone triggers melanogenesis via activation of the aryl hydrocarbon receptor pathway in B16F10 mouse melanoma cells. Int J Toxicol. 2021; 40(2):153–60. DOI:10.1177/1091581820987548
8. Pilotto A, Custodero C, Maggi S, Polidori MC, Veronese N, Ferrucci L. A multidimensional approach to frailty in older people. Ageing Res Rev 2020; 60:101047. DOI:10.1016/j.arr.2020.101047
9. Pavlović M, Jovanović I, Pavlović S, Stojanović V, Živković V, Bakić M, et al; Morphometric study of connective tissue in the human pituitary during aging process. Acta Facultatis Medicae Naissensis 2013; 30(2):79–84. DOI:10.2478/v10283-012-0040-4
10. Pavlović M, Jovanović I, Ugrenović S, Stojanović V, Živković V, Kundalić B, et al; Human anterior pituitary's ACTH cells during the aging process: immunohistochemic and morphometric study. Anat Sci Int. 2021; 96(2): 250–7. DOI: 10.1007/s12565-020-00583-7
11. van der Spoel E, Roelfsema F, van Heemst D. Relationships between 24-hours LH and testosterone concentrations and with other pituitary hormones in healthy older men. Journal of the Endocrine Society 2021; 5(9):1–15. DOI:10.1210/jendso/bvab075
12. Čukuranović-Kokoris J, Jovanović I, Ugrenović S, Stojanović V, Pavlović M, Kundalić B, et al; Immunohistochemical and morphometric study of adenohypophyseal gonadotropic cells in male cadavers of different ages. Acta Medica Medianae 2020; 59(4):49–61. DOI:10.5633/amm.2020.0407
13. Čukuranović-Kokoris J, Ajdžanović V, Pendovski L Ristić N, Mlošević V, Dovenska M, et al; The effects of long-term exposure to moderate heat on rat pituitary ACTH cells: Histological and hormonal study. Acta Vet (Beograd) 2022a; 72(1):1–15. DOI:10.2478/acve-2022-0001
14. Čukuranović-Kokoris J, Đorđević M, Jovanović I, Kundalić B, Pavlović M, Graovac I, et al: Morphometric analysis of somatotropic and folliculostellate cells of human anterior pituitary during ageing. Srp Arh Celok Lek. 2022b;50(5-6):274–81. DOI:10.2298/SARH211214044C
15. Čukuranović-Kokoris J, Ružić Z, Kanački Z, Stojanović S, Paraš S, Milošević V. Effects of vitamin C and early-age thermal conditioning on pituitary adrenocorticotropic hormone cells in broilers chronically exposed to heat stress: an immunohistomorphometric and hormonal study. Veterinary Research Forum. 2024; 15(3):125–30. DOI:10.30466/vrf.2023.2009320.3981
16. Keenan DM, Hefti JP, Veldhuis JD, Von Wolff M. Regulation and adaptation of endocrine axes at high altitude. Am J Physiol Endocrinol Metab. 2020 318(2):297–309. DOI:10.1152/ajpendo.00243.2019
17. Jovanović I, Ugrenović S, Ljubomirović M, Vasović LJ, Cukuranović R, Stefanović V. Folliculo-stellate cells - potential mediators of the inflammaging-induced hyperactivity of the hypothalamic-pituitary-adrenal axis in healthy elderly individuals. Med Hypotheses 2014; 83(4):501–5. DOI:10.1016/j.mehy.2014.08.018
18. Čukuranović-Kokoris J, Jovanović I, Pantović V, Krstić M, Stanojković M, Milošević V, et al; Morphometric analysis of the folliculostellate cells and luteinizing hormone gonadotropic cells of the anterior pituitary of the men during the aging process. Tissue and Cell 2017; 49(1): 78–85. DOI:10.1016/j.tice.2016.11.006
19. Ajdžanović V, Trifunović S, Miljić D, Šošić-Jurjević B, Filipović B, Miler M, et al: Somatopause, weaknesses of the therapeutic approaches and the cautious optimism based on experimental ageing studies with soy isoflavones. EXCLI Journal 2018; 17:279–301. DOI:10.17179/excli2017-956
20. Kelberman D, Rizzoti K, Lovell-Badge R, Robinson IC, Dattani MT. Genetic regulation of pituitary gland development in human and mouse. Endocr Rev 2009; 30 (7):790–829. DOI:10.1210/er.2009-0008
21. Baisre de León A. Histopathology of the pituitary lesions. Otolaryngol Clin North Am. 2022; 55(2):265–85. DOI:10.1016/j.otc.2021.12.003
22. Rudman D, Kutner M H, Rogers C M, Lubin M F, Fleming G A, Bain R P. Impaired growth hormone secretion in the adult population: relation to age and adiposity. J Clin Invest. 1981;67(5):1361–9. DOI:10.1172/jci110164
23. Sattler FR. Growth hormone in the aging male. Best Pract Res Clin Endocrinol Metab 2013; 27(4):541–55. DOI:10.1016/j.beem.2013.05.003
24. Adamo ML, Farrar RP. Resistance training, and IGF involvement in the maintenance of muscle mass during the aging process. Ageing Res Rev 2006;5(3):310–31. DOI:10.1016/j.arr.2006.05.001
25. Demiral M, Karaca MS , Unal E, Baysal B, Baran R, Demirbilek H, et al; A novel diagnostic tool for the evaluation of hypothalamic-pituitary region and diagnosis of growth hormone deficiency: pons ratio. J Pediatr Endocrinol Metab. 2020; 33(6):735–42. DOI:10.1515/jpem-2019-0321
26. Milošević V, Brkić B, Velkovski S, Sekulić M, Lovren M, Starčević V, et al; Morphometric and Functional changes of rat pituitary somatotropes and lactotropes after central administration of somatostatin. Pharmacology 1998; 57(1):28–34. DOI:10.1159/000028223
27. Veldhuis JD. Aging and hormones of the hypothalamo-pituitary axis: gonadotropic axis in men and somatotropic axes in men and women. Ageing Res Rev 2008; 7(3):189–208. DOI:10.1016/j.arr.2007.12.005
28. Perrini S, Laviola L, Carreira MC, Cignarelli A, Natalicchio A, Giorgino F. The GH/IGF1 axis and signaling pathways in the muscle and bone: mechanisms underlying age-related skeletal muscle wasting and osteoporosis. J Endocrinol 2010; 205(3):201–10. DOI:10.1677/JOE-09-0431
29. Antić VM, Stefanović N, Jovanović I, Antić M, Milić M, Krstić M, et al;. Morphometric analysis of somatotropic cells of the adenohypophysis and muscle fibers of the psoas muscle in the process of aging in humans. Ann Anat 2015; 200:44–53. DOI:10.1016/j.aanat.2015.01.006
30. Pamphlett R, Jew SK, Doble PA, Bishop DP. Elemental analysis of aging human pituitary glands implicates mercury as a contributor to the somatopause. Front Endocrinol (Lausanne). 2019;10:419. DOI:10.3389/fendo.2019.00419
31. Veldhuis JD. Changes in pituitary function with ageing and implications for patient care. Nat Rev Endocrinol. 2013;9(4):205–15. DOI:10.1038/nrendo.2013.38
32. Childs GV. Cytochemical studies of multifunctional gonadotropes. Microsc Res Tech 1997;39 (2):114e130. DOI:10.1002/(SICI)1097-0029(19971015)39:2
33. Grumbach MM, A window of opportunity: The diagnosis of gonadotropin deficiency in the male infant, J Clin Endocrinol Metab 2005;90(5):3122–7. DOI:10.1210/jc.2004-2465
34. Seminara SB, Hayes FJ, Crowley WF Jr. Gonadotropin releasing hormone deficiency in the human (idiopathic hypogonadotropic hypogonadism and Kallmann’s syndrome): Pathophysiological and genetic considerations. Endocr Rev 1998;19(5):521–39. DOI:10.1210/edrv.19.5.0344
35. Uwaifo GI. The Human Hypothalamus. Contemporary Endocrinology 2021; pp.1–528. DOI:10.1007/978-3-030-62187-2
36. Brioude F, Bouligand J, Trabado S., Francou B, Salenave S, Kamenicky P, et al; Non-syndromic congenital hypogonadotropic hypogonadism: Clinical presentation and genotypephenotype relationships. Eur J Endocrinol 2010; 162(5):835–51. DOI:10.1530/EJE-10-0083
37. Grumbach M.M. The neuroendocrinology of human puberty revisited. Horm Res 2002;57 (Suppl 2):2–14. DOI:10.1159/000058094
38. Bhasin S, Calof OM., Storer TW, Lee ML, Mazer NA, Jasuja R, et al:. Drug insight: Testosterone and selective androgen receptor modulators as anabolic therapies for chronic illness and aging. Nat Clin Pract Endocrinol Metab 2006; 2(3):146–59. DOI:10.1038/ncpendmet0120
39. Kaiser U. B. Gonadotropin Hormones. The Pituitary 2011; pp. 205–260. DOI:10.1016/b978-0-12-380926-1.10007-0
40. Roelfsema F, Liu PY, Takahashy PY, Yang RJ, Veldhuis JD. Dynamic interactions betwen LH and testosterone in healthy community-dwelling men: impact of age and body composition. J Clin Endocrinol Metab 2020; 105(3):628–41. DOI:10.1210/clinem/dgz246
41. Herman-Bonert VS, Melmed S. Growth Hormone. The Pituitary 2011;83–117. DOI:10.1016/b978-0-12-380926-1
42. Dudek P, Kozakowski J, Zgliczynski W. Late-onset hypogonadism. Menopause Rev 2017;16(2): 66–9. DOI:10.5114/pm.2017.68595
43. Veldhuis JD, Keenan D, Iranmanesh A, Takahashi P, Nehra A. The Ensemble Male Hypothalamo-Pituitary-Gonadal Axis. In: Timiras PS, editor. Physiological Basis of Aging and Geriatrics. 4th ed. CRC Press 2007; pp. 185–203. DOI:10.3109/9781420007091-14
44. Perez-Castro C, Renner U, Haedo MR, Stalla GK, Arzt E. Cellular and molecular specificity of pituitary gland physiology. Physiol Rev 2012; 92(1):1–38. DOI:10.1152/physrev.00003.2011
45. Nestorović N, Ristić N, Ajdžanović V, Trifunović S, Milošević V. Morphological and functional changes of pituitary GH and PRL cells following prolonged exposure of female rats to constant light. Experimental and Applied Biomedical Research 2023; 24(3):219–25. DOI:10.2478/sjecr-2019-0063
46. Takashi S. Heterogeneity and development of somatotropes and mammotropes in the rat. Zool Sci 1992;9:901–24.
47. Kurosumi K. Ultrastructural immunocytochemistry of the adenohypophysis in the rat: a review. J Electron Microsc Tech 1991;19(1): 42–56. DOI:10.1002/jemt.1060190105
48. Čukuranović-Kokoris J, Marković Filipović J, Đorđević M, Kundalić B, Stojanović V, Trandafilović M, Graovac I, Milošević V, Čukuranović R. Correlation analysis of pituitary lutheinizing and somatotropic cells in man during aging. Acta medica Medianae 2024; 63(1):90–6. DOI:10.5633/amm.2024.0110
49. Horvath E, Kovacs K. Ultrastructural diagnosis of human pituitary adenomas. Microsc Res Tech 1992; 20(2):107–35. DOI:10.1002/jemt.1070200202
Published
2024/11/13
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Copyright (c) 2024 Jovana Čukuranović Kokoris, Braca Kundalić, Miljana Pavlović, Slađana Ugrenović
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