Skip to main content

Advertisement

SpringerLink
Log in

Effects of intracranial surgery on pineal lipid droplets, on other structures, and on melatonin secretion

  • Original Article
  • Published:
Anatomical Science International Aims and scope Submit manuscript

Abstract

Unique effects of sham-pinealectomy [intracranial surgery (IS)] which include reduced functional activity of the adrenal gland and suppressed circadian rhythms of the adrenal medulla, and which are reversed by pinealectomy, have been reported in rodents. To clarify the mechanisms, we investigated whether or what changes occur in pineal functional activity after IS. Sixty-six male rats of normal and IS groups were used at 50 days of age. The pineal gland was first examined by quantitative electron microscopy. The Sudan III-stained lipid droplet content of the pinealocytes and plasma melatonin level were then investigated using the same animals. In IS rats, the lipid droplet content of the pinealocytes decreased in both the dark and light phases 14 days after surgery. Mean volumetric ratio of nucleus, nucleolus, and mitochondria tended to increase in IS rats. The mean plasma concentration of melatonin showed apparent day–night changes, but no significant changes because of IS, 36 h and 14 days after surgery. But in the dark phase 14 days after surgery, plasma melatonin levels showed increased dispersion of values (P < 0.04). Thus, after IS the lipid content of pinealocytes showed changes not closely related to those of plasma melatonin level. From these and other results it is speculated that IS effects are dissimilar to usual stress responses, that day–night rhythms of functional activities of the pineal and adrenal medulla are differently controlled, and that pineal gland-dependent IS effects are most probably induced by changed sensitivity/states of target mechanisms to the pineal hormone melatonin.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Benitez-King G, Huerto-Delgadillo L, Anton-Tay F (1993) Binding of 3H-melatonin to calmodulin. Life Sci 53:201–217

    Article  PubMed  CAS  Google Scholar 

  • Burnstock G (2007) Physiology and pathophysiology of purinergic neurotransmission. Physiol Rev 87:659–797

    Article  PubMed  CAS  Google Scholar 

  • Cardinali DP, Ritta MN, Fuentes AM et al (1980) Prostaglandin E release by rat medial basal hypothalamus in vitro: inhibition by melatonin at submicromolar concentrations. Eur J Pharmacol 67:151–153

    Article  PubMed  CAS  Google Scholar 

  • Dagnino-Subiabre A, Zepeda-Carreno R, Diaz-Veliz G, Mora S, Aboitiz F (2006) Chronic stress induces upregulation of brain-derived neurotrophic factor (BDNF) mRNA and integrin α5 expression in the rat pineal gland. Brain Res 1086:27–34

    Article  PubMed  CAS  Google Scholar 

  • Deussen-Schmitter M, Garweg G, Schwabedal PE, Wartenberg H (1976) Simultaneous changes of the perivascular contact area and HIOMT activity in the pineal organ after bilateral adrenalectomy in the rat. Anat Embryol 149:297–305

    Article  PubMed  CAS  Google Scholar 

  • Dill RE (1961) The effects of pinealectomy or pineal extracts on corticosterone secretion in the rat. Anat Rec 139:222 (Abstract)

    Google Scholar 

  • Edvinsson L, MacKenzie ET, McCulloch J (1993) Cerebral blood flow and metabolism. Raven Press, New York, pp 421–422, 450–451, 569

  • Frowein A, Lapin V (1979) Effects of sham-pinealectomy, performed under white and red light, on the melatonin content of rat pineal glands. Experientia 35:1681

    Article  PubMed  CAS  Google Scholar 

  • Funk CD (2001) Prostaglandins and leukotrienes: advances in eicosanoid biology. Science 294:1871–1875

    Article  PubMed  CAS  Google Scholar 

  • Ganong WF (2005) Review of medical physiology, 22 edn. McGraw–Hill, New York, pp 307–310, 356–381, 611–620

  • Hökfelt T, Johansson O, Ljungdahl A, Lundberg JM, Schultzberg M (1980) Peptidergic neurons. Nature 284:515–521

    Article  PubMed  Google Scholar 

  • Irie T, Kachi T (1999) A quantitative histological study on neuronal cell nuclei in lateral and ventral horns of the rat spinal cord: Effects of intracranial surgery, pinealectomy and continuous lighting. Hirosaki Med J 51:15–26

    Google Scholar 

  • Kachi T (1987) Pineal actions on the autonomic system. Pineal Res Rev 5:217–263

    CAS  Google Scholar 

  • Kachi T (2007) Pineal structures and functions in mammalian body mechanisms coping with exogenous and endogenous changes. Hirosaki Med J 59(Suppl):S262–S277

    CAS  Google Scholar 

  • Kachi T, Quay WB (1984) Seasonal changes in glycogen level and size of pinealocytes of the white-footed mouse, Peromyscus leucopus: a semiquantitative histochemical study. J Pineal Res 1:163–174

    Article  PubMed  CAS  Google Scholar 

  • Kachi T, Banerji TK, Quay WB (1979) Daily rhythmic changes in synaptic vesicle contents of nerve endings on adrenomedullary adrenaline cells, and their modification by pinealectomy and sham operations. Neuroendocrinology 28:201–211

    Article  PubMed  CAS  Google Scholar 

  • Kachi T, Banerji TK, Quay WB (1984) Quantitative cytological analysis of functional changes in adrenomedullary chromaffin cells in normal, sham- operated and pinealectomized rats in relation to time of day: I. nucleolar size. J Pineal Res 1:31–49

    Article  PubMed  CAS  Google Scholar 

  • Kachi T, Banerji TK, Quay WB (1985) Quantitative ultrastructural analysis of differences in adrenomedullary chromaffin cells of golden hamsters related to time of day, pinealectomy, and intracellular region. J Pineal Res 2:253–269

    Article  PubMed  CAS  Google Scholar 

  • Kachi T, Takahashi G, Banerji TK, Quay WB (1992) Rough endoplasmic reticulum in the adrenaline and noradrenaline cells of the adrenal medulla: effects of intracranial surgery and pinealectomy. J Pineal Res 12:89–95

    Article  PubMed  CAS  Google Scholar 

  • Kachi T, Takahashi G, Suzuki T et al (1993) Effects of pineal and intracranial surgery on the adrenal medulla:quantitative morphological and immunohistochemical studies. In: Touitou Y, Arendt J, Pevet P (eds) Melatonin and the pineal gland. Excerpta Medica, Amsterdam, pp 277–280

    Google Scholar 

  • Kachi T, Takahashi G, Suzuki T et al (1997) Pineal effects on adrenal medulla, area postrema and brain water content in relation to intracranial surgery. Biol Signals 6:255–263

    Article  PubMed  CAS  Google Scholar 

  • Kachi T, Takahashi G, Suzuki T et al (1998) Dynamic and versatile structures of adrenal medulla, related to pineal and surgery. In: Yagihashi S, Kachi T, Wakui M (eds) Dynamic cells: cell biology of the 21st century. Elsevier, Amsterdam, pp 47–58

    Google Scholar 

  • Kachi T, Tanaka D, Watanabe S, Suzuki R, Tonosaki Y, Fujieda H (2006) Physiological pineal effects on female reproductive function of laboratory rats: prenatal development of pups, litter size and estrous cycle in middle age. Chronobiol Int 23:289–300

    Article  PubMed  CAS  Google Scholar 

  • Kimura N, Kachi T (1996) Effects of time of day, intracranial surgery and pineal hormone on methionine-enkephaline-like immunoreactivity in adrenal medullae of golden hamsters. Hirosaki Med J 48:139–147

    CAS  Google Scholar 

  • Kudou H, Kachi T, Suzuki T, Saito Y (2001) Effects of pinealectomy on the area postrema in rats: a quantitative histological study with special reference to capillaries and neuronal cell nuclei. Arch Histol Cytol 64:139–148

    Article  PubMed  CAS  Google Scholar 

  • Lezoualc’h F, Aparapani M, Behl C (1998) N-acetyl-serotonin (normelatonin) and melatonin protect neurons against oxidative challenges and suppress the activity of the transcription factor NF-kappa B. J Pineal Res 24:168–178

    Article  PubMed  CAS  Google Scholar 

  • Lynch HJ, Deng MH (1986) Pineal responses to stress. J Neural Transm 21:461–473

    CAS  Google Scholar 

  • Meyer DC, Quay WB (1976) Effects of continuous light and darkness, and of pinealectomy, adrenalectomy and gonadectomy on uptake of 3H-serotonin by the suprachiasmatic nuclear region of male rats. Neuroendocrinology 22:231–239

    Article  PubMed  CAS  Google Scholar 

  • Miline R, Krstic R, Devecerski V (1968) Sur le comportement de la glande pineale dans des conditions de stress. Acta Anat 71:352–402

    Article  PubMed  CAS  Google Scholar 

  • Møller M, Baeres FMM (2002) The anatomy and innervation of the mammalian pineal gland. Cell Tissue Res 309:139–150

    Article  PubMed  CAS  Google Scholar 

  • Morton DJ, Reiter RJ, Buzzel GR (1989) Swimming-induced suppression of rat pineal melatonin is prevented by pretreatment with calcium channel blockers. Proc Soc Exp Biol Med 190:105–108

    PubMed  CAS  Google Scholar 

  • Nishimura S, Fujino Y, Shimaoka M, Hagihira S, Taenaka N, Yoshiya I (1998) Circadian secretion patterns of melatonin after major surgery. J Pineal Res 25:73–77

    Article  PubMed  CAS  Google Scholar 

  • Oishi K, Murai I, Sakamoto K et al (2000) The pineal gland is not essential for circadian expression of rat period homologue (rper2) mRNA in the suprachiasmatic nucleus and peripheral tissues. Brain Res 885:298–302

    Article  PubMed  CAS  Google Scholar 

  • Owens DW, Gern WA (1985) The pineal gland and melatonin in sea turtles. In: Lofts B, Holmes WN (eds) Current trends in comparative endocrinology. Hong Kong University Press, Hong Kong, pp 645–648

    Google Scholar 

  • Pang SF, Tsang CW, Hong GX, Yip PCY, Tang PL, Brown GM (1990) Fluctuation of blood melatonin concentrations with age: result of changes in pineal melatonin secretion, body growth, and aging. J Pineal Res 8:179–192

    Article  PubMed  CAS  Google Scholar 

  • Quay WB (1974) Pineal chemistry in cellular and physiological mechanisms. Charles C Thomas, Springfield, pp 21–34, 63–102, 137–200, 323–332

  • Quay WB, Payer AF, Parkening TA, Banerji TK, Collins TJ (1982) Melatonin’s inhibition of pituitary, adrenal testicular and accessory gland growth in male golden hamsters: pineal dependence and organ differences with shielding and intracranial surgery. J Neural Transm 53:59–73

    Article  PubMed  CAS  Google Scholar 

  • Reiter RJ, Melchiorri D, Se werynek E et al (1995) A review of the evidence supporting melatonin’s role as an antioxidant. J Pineal Res 18:1–11

    Article  PubMed  CAS  Google Scholar 

  • Sato T (1968) A modified method for lead staining of thin sections. J Electr Microsc 17:158–159

    CAS  Google Scholar 

  • Selye H (1976) The stress of life. Revised ed. McGraw–Hill, New York

    Google Scholar 

  • Sharman R, McMillan CR, Tenn CC, Niles LP (2006) Physiological neuroprotection by melatonin in a 6-hydroxydopamine model of Parkinson’s disease. Brain Res 1068:230–236

    Article  CAS  Google Scholar 

  • Simonneaux V, Ouichou A, Pevet P (1993) Pituitary adenylate cyclase activating polypeptide (PACAP) stimulate melatonin synthesis from the rat pineal gland. Brain Res 603:148–152

    Article  PubMed  CAS  Google Scholar 

  • Spitzer NC, Sejnowski TJ (1997) Biological information processing: bits of progress. Science 277:1060–1061

    Article  PubMed  CAS  Google Scholar 

  • Suzuki T, Takahashi G, Kachi T (1999) Quantitative electron-microscopic study on glial cells in contact with the perivascular space in the rat pineal gland: effects of intracranial surgery. J Aomori Univ Health Welf 1:133–137

    Google Scholar 

  • Vaughan GM, McDonald SD, Jordan RM et al (1978) Melatonin concentration in human blood and cerebrospinal fluid: relationship to stress. J Clin Endocr Metab 47:220–223

    PubMed  CAS  Google Scholar 

  • Vaughan GM, Bell R, de la Peña A (1979) Nocturnal plasma melatonin in human: episodic pattern and influence of light. Neurosci Lett 14:81–84

    Article  PubMed  CAS  Google Scholar 

  • Vollrath L (1981) Handbuch der mikroskopischen Anatomie des Menschen. Vol. VI, 7 The pineal organ. Springer, Berlin, pp 71–174, 399–436, 476–478

  • Weibel ER, Kistler GS, Scherle WF (1966) Practical stereological methods for morphometric cytology. J Cell Biol 30:23–38

    Article  PubMed  CAS  Google Scholar 

  • Wurtman RJ, Axelrod J, Kelly DE (1968) The pineal. Academic Press, New York, London, pp 1–46, 108–144

Download references

Acknowledgments

This work was supported in part by the Karoji Memorial Fund for Medical Research in Hirosaki University, Japan, granted to T. Kachi. We are grateful to Professor K. Shoumura, Department of Neuroanatomy, Cell Biology, and Histology, Professor S. Motomura and Associate Professor K.-I. Furukawa, Department of Pharmacology, and Professor H. Ohkuma and Dr. K. Asano, Department of Neurosurgery, Hirosaki University Graduate School of Medicine, for helpful discussion and advice, and also to Mr F. Henault (formerly of Hirosaki University, Hirosaki, Japan) for his reading and correction of the manuscript.

Author information

Author notes

  1. Michihiro Kurushima

    Present address: Department of Surgery, Aomori Central Hospital, Higashitsukurimichi 2-1-1, Aomori, 030-8553, Japan

  2. Gen Takahashi

    Present address: , Shinteramachi 39-16, Hirosaki, 036-8214, Japan

  3. Takao Suzuki

    Present address: Department of Physical Therapy, Faculty of Health Sciences, Aomori University of Health and Welfare, Mase 58-1, Hamadate, Aomori, 030-8505, Japan

Authors and Affiliations

  1. Department of Anatomical Science, Hirosaki University Graduate School of Medicine, Zaifucho 5, Hirosaki, 036-8562, Japan

    Michihiro Kurushima, Gen Takahashi, Takao Suzuki & Takashi Kachi

  2. Department of Physiology, Hokkaido University Graduate School of Medicine, Sapporo, Japan

    Satoko Hashimoto & Ken-ichi Honma

Authors
  1. Michihiro Kurushima
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Gen Takahashi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Takao Suzuki
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Satoko Hashimoto
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Ken-ichi Honma
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Takashi Kachi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Takashi Kachi.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kurushima, M., Takahashi, G., Suzuki, T. et al. Effects of intracranial surgery on pineal lipid droplets, on other structures, and on melatonin secretion. Anat Sci Int 84, 17–26 (2009). https://doi.org/10.1007/s12565-008-0004-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12565-008-0004-z

Keywords

Search

Navigation