Postnatal Development of the Lumbar Para-Aortic Paraganglion
https://doi.org/10.18499/2225-7357-2025-14-2-53-62
Abstract
So far, a number of contradictory data have accumulated regarding not only the timing and characteristics, but also the very fact of age-related involution of the largest of the extra-adrenal chromaffin paraganglia – the lumbar para-aortic paraganglion (LPP, organ of Zuckerkandl). The aim is to investigate the features of age-related transformations of the LPP in postnatal ontogenesis. Material and methods. Using histological and histochemical methods on complete serial sections, the organ complexes of the area of location of the LPP of rats in the main periods of postnatal ontogenesis (0–1, 7–8, 14, 21 days, 1, 3, 6–8, 14 months and 2 years). Results. All newborn animals have a well-developed LPP, which contains arrays of chromaffin cells with a moderate chromaffin reaction and heterogeneous groups of slightly differentiated cells. The size and number of chromaffin cells in the LPP decrease (according to a number of signs via autophagy) while the presence of nerve cells increases from the end of the 1st postnatal week. This leads to the transformation of the LPP into a mixed chromaffin-nerve ganglion, then into a typical nerve ganglion. Chromaffin cells in the LPP area completely disappear by the 1st month. Groups of chromaffin cells with intense chromaffin reaction reappear in the LPP area nerve ganglia starting from 3 months, then their number and size increase until old age. We associate the causes of age-related LPP involution with the activation of adrenal medulla maturation during the same period and the secondary appearance and hypertrophy of chromaffin cells in the LPP area with increased stress effects during maturation and weakening of the cardiovascular system during aging. Both factors cause an increase in the level of glucocorticoids which are stimulators of the proliferation of extra-adrenal chromaffin tissue. Conclusion. The rat LPP demonstrate a pronounced age-related involution, accompanied by the replacement of chromaffin tissue by nervous tissue from the 1st to the 4th postnatal weeks. After the completion of age-related involution of the LPP, clusters of chromaffin cells appear for the second time in the nerve ganglia of this area, progressing as growing up and ages.
About the Author
K. G. KemoklidzeRussian Federation
Konstantin G. Kemoklidze – Cand. Sci. (Biol.), Associate Professor at the Department of Histology, Cytology, and Embryology
ul. Revolyutsionnaya, 5, Yaroslavl, 150000
References
1. Bondarenko NS, Murtazina AR, Dil'mukhametova LK, Ikonopistseva MA, Volina EV, Ugryumov MV. Sekretornaya aktivnost' mozga i perifericheskikh organov: spontannoe i stimulirovannoe vydelenie noradrenalina v ontogeneze krys. Doklady Akademii nauk. 2016;467(6):721–724. (In Russ.).
2. Bondarenko NS, Dil'mukhametova LK, Kurina AYu, Murtazina AR, Sapronova AYa, Sysoeva AP, Ugryumov MV. Plastichnost' tsentral'nykh i perifericheskikh istochnikov noradrenalina v ontogeneze u krys. Biokhimiya. 2017;82(3):519–527. (In Russ.).
3. Deev RV, Bilyalov AI, Zhampeisov TM. Sovremennye predstavleniya o kletochnoi gibeli. Geny i kletki. 2018;13(1):6–19. (In Russ.).
4. Murtazina AR, Nikishina YuO, Bondarenko NS, Sapronova AYa, Ugryumov M.V. Signal'nye molekuly v razvitii organizma: tsentral'nye i perifericheskie istochniki noradrenalina v ontogeneze krys. Doklady Akademii nauk. 2016;466(6):730–733. (In Russ.).
5. Murtazina AR, Nikishina YuO, Bondarenko NS, , Sapronova AYa, Volina EV, Ugryumov MV. Ekspressiya fermentov sinteza noradrenalina v organe Tsukerkandlya v kriticheskii period morfogeneza u krys. Doklady Akademii nauk. 2017;474(3):382–385. (In Russ.).
6. Murtazina AR, Nikishina YuO, Dil'mukhametova LK, Sapronova AYa, Ugryumov MV. Rol' mozga v regulyatsii perifericheskikh noradrenalin-produtsiruyushchikh organov v period morfogeneza u krys. Doklady Akademii nauk. 2019;486(6):748–752. (In Russ.).
7. Pavlov AV, Kemoklidze KG. Tsitologicheskie mekhanizmy postnatal'nogo rosta khromaffinnoi tkani nadpochechnika. Ontogenez. 1998;29(2):23–128. (In Russ.).
8. Rumyantseva TA Vozrastnye preobrazovaniya morfometricheskikh i gistokhimicheskikh kharakteristik neirotsitov razlichnykh gangliev u belykh krys. Morfologiya. 2004;125(3):40–45. (In Russ.).
9. Semashko MI. K voprosu o vyyavlenii noradrenalin- i adrenalinsekretiruyushchikh kletok mozgovogo veshchestva nadpochechnikov laboratornykh zhivotnykh i cheloveka. Arkhiv anatomii, gistologii i embriologii. 1977;73(7):37– 41. (In Russ.).
10. Smitten NA. Simpatoadrenalovaya sistema v filo- i ontogeneze pozvonochnykh. M.: Nauka; 1972: 348. (In Russ.).
11. Fokanova OA, Rumyantseva TA. Vozrastnye preobrazovaniya kletochnogo sostava bol'shogo tazovogo gangliya u krys v norme i pri desimpatizatsii. Morfologiya. 2014;146(6):42–46. (In Russ.).
12. Shlyapina VL, Yurtaeva SV, Rubtsova MP, Dontsova OA. Na rasput'e: mekhanizmy apoptoza i autofagii v zhizni i smerti kletki. Acta Naturae. 2021;13(2):106–115. (In Russ.).
13. Ahonen M., Soinila S., Joh T. H. Pre- and postnatal development of rat retroperitoneal paraganglia. J Auton Nerv Syst. 1987;18(2):111– 120.
14. Ambriz-Tututi M, Monjaraz-Fuentes F, Drucker-Colín R. Chromaffin cell transplants: from the lab to the clinic. Life Sci. 2012 Dec 17;91(25-26):1243-51. doi: 10.1016/j.lfs.2012.10.012.
15. Böck P. The paraganglia. In: A. Oksche, L. Vollrath. Handbuch der mikroskopischen Anatomie des Menschen. Berlin: Springer; 1982:6(8).
16. Ciaranello RD, Axelrod J. Effects of dexamethasone of neurotransmitter enzymes in chromaffin tissue of the newborn rat. J Neurochem. 1975 Apr;24(4):775-8.
17. Coupland RE. The natural history of the chromaffin cell--twenty-five years on the beginning. Arch Histol Cytol. 1989;52 Suppl:331-41. doi: 10.1679/aohc.52.suppl_331.
18. De Gallardo MR, Freire F, Tramezzani JH. The organ of Zuckerkandl of the newborn rat and its postnatal involution. Acta Physiol Lat Am. 1974;24(4):290-304. 19. Disick GI, Palese MA. Extra-adrenal pheochromocytoma: diagnosis and management. Curr Urol Rep. 2007 Jan;8(1):83-8. doi: 10.1007/s11934-007-0025-5.
19. Eränkö L, Eränkö O. Effect of hydrocortisone on histochemically demonstrable catecholamines in the sympathetic ganglia and extra-adrenal chromaffin tissue of the rat. Acta Physiol Scand. 1972 Jan;84(1):125-33. doi: 10.1111/j.1748-1716.1972.tb05161.x.
20. Espejo EF, Gonzalez-Albo MC, Moraes JP, El Banoua F, Flores JA, Caraballo I. Functional regeneration in a rat Parkinson's model after intrastriatal grafts of glial cell line-derived neurotrophic factor and transforming growth factor beta1-expressing extra-adrenal chromaffin cells of the Zuckerkandl's organ. J Neurosci. 2001 Dec 15;21(24):9888-95. doi: 10.1523/JNEUROSCI.21-24-09888.2001.
21. Fulenwider H. D., Caruso M. A., Ryabinin A.E. Manifestations of domination: Assessments of social dominance in rodents. Genes Brain Behav. 2022; 21 (3): Artickle e12731.
22. Galan-Rodriguez B, del-Marco A, Flores JA, Ramiro-Fuentes S, Gonzalez-Aparicio R, Tunez I, Tasset I, Fernandez-Espejo E. Grafts of extra-adrenal chromaffin cells as aggregates show better survival rate and regenerative effects on parkinsonian rats than dispersed cell grafts. Neurobiol Dis. 2008 Mar;29(3):529-42. doi: 10.1016/j.nbd.2007.11.009.
23. Honoré LH. A light microscopic method for the differentiation of noradrenaline- and adrenaline-producing cells of the rat adrenal medulla. J Histochem Cytochem. 1971 Aug;19(8):483-6. doi: 10.1177/19.8.483.
24. Kastriti ME, Kameneva P, Kamenev D, Dyachuk V, Furlan A, Hampl M, Memic F, Marklund U, Lallemend F, Hadjab S, Calvo-Enrique L, Ernfors P, Fried K, Adameyko I. Schwann Cell Precursors Generate the Majority of Chromaffin Cells in Zuckerkandl Organ and Some Sympathetic Neurons in Paraganglia. Front Mol Neurosci. 2019 Jan 25;12:6. doi: 10.3389/fnmol.2019.00006.
25. Lempinen M, Extra-adrenal chromaffin tissue of the rat and the effect of cortical hormones on it. Acta Physiol Scand Suppl. 1964;62(231):1–91. 27. Masoro EJ. Glucocorticoids and aging. Aging (Milano). 1995 Dec;7(6):407-13. doi: 10.1007/BF03324354.
26. McDonald DM, Blewett RW. Location and size of carotid body-like organs (paraganglia) revealed in rats by the permeability of blood vessels to Evans blue dye. J Neurocytol. 1981 Aug;10(4):607-43. doi: 10.1007/BF01262593.
27. Partanen M, Chiueh CC, Rapoport SI. Age related increase in catecholamine-containing paraganglia in male Fischer-344 rats. Anat Rec. 1981 Nov;201(3):563-6. doi: 10.1002/ar.1092010312.
28. Partanen M, London ED, Rapoport SI. Glucose utilization in sympathetic ganglia of male Fischer-344 rats at different ages. J Auton Nerv Syst. 1982 May;5(3):391-8. doi: 10.1016/0165-1838(82)90080-7.
29. Partanen M, Hervonen A, Rapoport SI. The ultrastructure of hypertrophied paraganglia in aged rats. J Anat. 1984 Dec;139 ( Pt 4)(Pt 4):619-26.
30. Partanen M, Linnoila I, Hervonent A, Rapoport SI. The effect of aging on extra-adrenal catecholamine storing cells of the rat. Neurobiol Aging. 1984 Summer;5(2):105-10. doi: 10.1016/0197-4580(84)90039-3.
31. Partanen M, Rapoport SI, Reis DJ, Joh TH, Stolk JM, Linnoila I, Teitelman G, Hervonen A. Catecholamine-synthesizing enzymes in paraganglia of aged Fischer-344 rats. Immunohistochemistry and fluorescence microscopy. Cell Tissue Res. 1984;238(2):217-20. doi: 10.1007/BF00217291.
32. Peters LL, Wood BG. The prenatal development of the organ of Zuckerkandl in rats. Life Sci. 1987 Sep 14;41(11):1355-9. doi: 10.1016/0024-3205(87)90609-6.
33. Ramiro-Fuentes S, del-Marco A, Galan-Rodriguez B, Ramirez-Ponce P, Fernandez-Espejo E. Morphophysiology of the Zuckerkandl's paraganglion: effects of dexamethasone and aging. Neurobiol Aging. 2010 Dec;31(12):2115-27. doi: 10.1016/j.neurobiolaging.2008.12.001.
34. Sapolsky RM. Do glucocorticoid concentrations rise with age in the rat? Neurobiol Aging. 1992 Jan-Feb;13(1):171-4. doi: 10.1016/0197-4580(92)90025-s.
35. Schober A, Parlato R, Huber K, Kinscherf R, Hartleben B, Huber TB, Schütz G, Unsicker K. Cell loss and autophagy in the extra-adrenal chromaffin organ of Zuckerkandl are regulated by glucocorticoid signalling. J Neuroendocrinol. 2013 Jan;25(1):34-47. doi: 10.1111/j.1365-2826.2012.02367.x.
36. Stein-Behrens BA, Sapolsky RM. Stress, glucocorticoids, and aging. Aging (Milano). 1992 Sep;4(3):197-210. doi: 10.1007/BF03324092.
37. Taatjes DJ, Sobel BE, Budd RC. Morphological and cytochemical determination of cell death by apoptosis. Histochem Cell Biol. 2008 Jan;129(1):33-43. doi: 10.1007/s00418-007-0356-9.
38. von Dalnok GK, Menssen HD. A quantitative electron microscopic study of the effect of glucocorticoids in vivo on the early postnatal differentiation of paraneuronal cells in the carotid body and the adrenal medulla of the rat. Anat Embryol (Berl). 1986;174(3):307-19. doi: 10.1007/BF00698781
Review
For citations:
Kemoklidze K.G. Postnatal Development of the Lumbar Para-Aortic Paraganglion. Journal of Anatomy and Histopathology. 2025;14(2):53-62. (In Russ.) https://doi.org/10.18499/2225-7357-2025-14-2-53-62