Publication Cover
Chronobiology International
The Journal of Biological and Medical Rhythm Research
Volume 34, 2017 - Issue 6
299
Views
11
CrossRef citations to date
0
Altmetric
Review

Perinatal light imprinting of circadian clocks and systems (PLICCS): A signature of photoperiod around birth on circadian system stability and association with cancer

ORCID Icon &
Pages 782-801 | Received 03 Jan 2017, Accepted 30 Mar 2017, Published online: 21 Apr 2017

References

  • Abraham U, Granada AE, Westermark PO, et al. 2010. Coupling governs entrainment range of circadian clocks. Mol Syst Biol. 6:438.
  • Ansorge MS, Zhou M, Lira A, et al. 2004. Early-life blockade of the 5-HT transporter alters emotional behavior in adult mice. Science. 306:879–81.
  • Bartsch H, Bartsch C, Mecke D, Lippert TH. 1994. Seasonality of pineal melatonin production in the rat: Possible synchronization by the geomagnetic field. Chronobiol Int. 11:21–26.
  • Basta NO, James PW, Craft AW, McNally RJ. 2010. Season of birth and diagnosis for childhood cancer in Northern England, 1968-2005. Paediatr Perinat Epidemiol. 24:309–18.
  • Bauer M, Glenn T, Alda M, et al. 2015. Influence of light exposure during early life on the age of onset of bipolar disorder. J Psychiatr Res. 64:1–8.
  • Benderlioglu Z, Dow E, Pyter LM. 2007. Neonatal exposure to short days and low temperatures blunts stress response and yields low fluctuating asymmetry in Siberian hamsters. Physiol Behav. 90:459–65.
  • Bishnupuri KS, Haldar C. 1999. Maternal photoperiodic exposures alter the neonatal growth, pineal functions and sexual development of the Indian palm squirrel F. pennanti. Short communication. J Neural Transm (Vienna). 106:869–81.
  • Boscoe FP, Schymura MJ. 2006. Solar ultraviolet-B exposure and cancer incidence and mortality in the United States, 1993-2002. BMC Cancer. 6:264.
  • Bosetti C, Bertuccio P, Chatenoud L, et al. 2010. Childhood cancer mortality in Europe, 1970-2007. Eur J Cancer. 46:384–94.
  • Brenner AV, Linet MS, Shapiro WR, et al. 2004. Season of birth and risk of brain tumors in adults. Neurology. 63:276–81.
  • Brooks E, Canal MM. 2013. Development of circadian rhythms: Role of postnatal light environment. Neurosci Biobehav Rev. 37:551–60.
  • Brooks E, Patel D, Canal MM. 2014. Programming of mice circadian photic responses by postnatal light environment. Plos One. 9:e97160.
  • Brown AS, Begg MD, Gravenstein S, et al. 2004. Serologic evidence of prenatal influenza in the etiology of schizophrenia. Arch Gen Psychiatry. 61:774–80.
  • Cambras T, Canal MM, Cernuda-Cernuda R, et al. 2015. Darkness during early postnatal development is required for normal circadian patterns in the adult rat. Chronobiol Int. 32:178–86.
  • Canal-Corretger MM, Vilaplana J, Cambras T, Diez-Noguera A. 2001a. Effect of light on the development of the circadian rhythm of motor activity in the mouse. Chronobiol Int. 18:683–96.
  • Canal-Corretger MM, Vilaplana J, Cambras T, Diez-Noguera A. 2001b. Functioning of the rat circadian system is modified by light applied in critical postnatal days. Am J Physiol Regul Integr Comp Physiol. 280:R1023–1030.
  • Choi NW, Hsu PH, Nelson NA, Abu-Zeid HA. 1977. Some descriptive epidemiologic features of central nervous system (CNS) neoplasms in childhood, in Manitoba, Canada. Neurol Neurocir Psiquiatr. 18:199–210.
  • Ciarleglio CM, Axley JC, Strauss BR, et al. 2011. Perinatal photoperiod imprints the circadian clock. Nat Neurosci. 14:25–27.
  • Coebergh JW, Reedijk AM, De Vries E, et al. 2006. Leukaemia incidence and survival in children and adolescents in Europe during 1978-1997. Report from the automated childhood cancer information system project. Eur J Cancer. 42:2019–36.
  • Cohen M, Lippman M, Chabner B. 1978. Role of pineal gland in aetiology and treatment of breast cancer. Lancet. 2:814–16.
  • Cole P, MacMahon B, Aisenberg A. 1968. Mortality from Hodgkin’s disease in the United States. Evidence for the multiple-aetiology hypothesis. Lancet. 2:1371–76.
  • Coste A, Goujon S, Boniol M, et al. 2015. Residential exposure to solar ultraviolet radiation and incidence of childhood hematological malignancies in France. Cancer Causes Control. 26:1339–49.
  • Criscione VD, Weinstock MA. 2007. Incidence of cutaneous T-cell lymphoma in the United States, 1973-2002. Arch Dermatol. 143:854–59.
  • Crump C, Sundquist J, Sieh W, et al. 2014. Season of birth and risk of Hodgkin and non-Hodgkin lymphoma. Int J Cancer. 135:2735–39.
  • Crump C, Sundquist J, Sieh W, et al. 2015. Perinatal risk factors for acute myeloid leukemia. Eur J Epidemiol. 30:1277–85.
  • De Zegher F, Styne DM, Daaboul J, et al. 1989. Hormone ontogeny in the ovine fetus and neonatal lamb. XX. Effect of age, breeding season, and twinning on the growth hormone (GH) response to GH-releasing factor: Evidence for a homeostatic role of fetal GH. Endocrinology. 124:124–28.
  • Deguchi T. 1975. Ontogenesis of a biological clock for serotonin: Acetylcoenzyme A N-acetyltransferase in pineal gland of rat. Proc Natl Acad Sci U S A. 72:2814–18.
  • DeLong ER, Maile MC, Grufferman S. 1984. Climate, socioeconomic status and Hodgkin’s disease mortality in the United States. J Chronic Dis. 37:209–13.
  • Diaz E, Vazquez N, Fernandez C, et al. 2011. Seasonal variations of Substance P in the striatum of the female rat are affected by maternal and offspring pinealectomy. Neurosci Lett. 492:71–75.
  • Eisler JA, Tannenbaum PL, Mann DR, Wallen K. 1993. Neonatal testicular suppression with a GnRH agonist in rhesus monkeys: Effects on adult endocrine function and behavior. Horm Behav. 27:551–67.
  • Erren TC. 2006. Low risks at high latitudes: Does the arctic hold clues to prostate cancer? Am J Prev Med. 31:273.
  • Erren TC, Gross JV, Meyer-Rochow VB. 2011a. Light, clocks, mood, and cancer: Consolidation and novel tests of latitude and instability hypotheses. Chronobiol Int. 28:471–73. author reply p 473.
  • Erren TC, Koch MS, Gross JV, et al. 2012a. A possible role of perinatal light in mood disorders and internal cancers: Reconciliation of instability and latitude concepts. Neuro Endocrinol Lett. 33:314–17.
  • Erren TC, Nise MS, Meyer-Rochow VB. 2011b. Latitude, light, clocks and mood. Psychopharmacology (Berl). 216:147–48.
  • Erren TC, Piekarski C. 1999. Does winter darkness in the Artic protect against cancer? The melatonin hypothesis revisited. Med Hypotheses. 53:1–5.
  • Erren TC, Reiter RJ. 2009a. Defining chronodisruption. J Pineal Res. 46:245–47.
  • Erren TC, Reiter RJ. 2009b. Light Hygiene: Time to make preventive use of insights–old and new–into the nexus of the drug light, melatonin, clocks, chronodisruption and public health. Med Hypotheses. 73:537–41.
  • Erren TC, Reiter RJ. 2013. Revisiting chronodisruption: When the physiological nexus between internal and external times splits in humans. Naturwissenschaften. 100:291–98.
  • Erren TC, Reiter RJ, Meyer-Rochow VB. 2012b. A perinatal signature of light on chronobiology? If so, numerous questions arise and experimental animal research must provide more information. Neuro Endocrinol Lett. 33:318–20.
  • Erren TC, Reiter RJ, Piekarski C. 2003. Light, timing of biological rhythms, and chronodisruption in man. Naturwissenschaften. 90:485–94.
  • Erren TC, Trautmann K, Salz MM, Reiter RJ. 2013. Newborn intensive care units and perinatal healthcare: On light’s imprinting role on circadian system stability for research and prevention. J Perinatol. 33:824–25.
  • Facchini U, Camnasio M, Cantaboni A, et al. 1985. Geographical variation of cancer mortality in Italy. Int J Epidemiol. 14:538–48.
  • Feltbower RG, Pearce MS, Dickinson HO, et al. 2001. Seasonality of birth for cancer in Northern England, UK. Paediatr Perinat Epidemiol. 15:338–45.
  • Foster RG, Roenneberg T. 2008. Human responses to the geophysical daily, annual and lunar cycles. Curr Biol. 18:R784–R794.
  • Fraumeni JF Jr., Li FP. 1969. Hodgkin’s disease in childhood: An epidemiologic study. J Natl Cancer Inst. 42:681–91.
  • Goto M, Oshima I, Tomita T, Ebihara S. 1989. Melatonin content of the pineal gland in different mouse strains. J Pineal Res. 7:195–204.
  • Green NH, Jackson CR, Iwamoto H, et al. 2015. Photoperiod programs dorsal raphe serotonergic neurons and affective behaviors. Curr Biol. 25:1389–94.
  • Halperin EC, Miranda ML, Watson DM, et al. 2004. Medulloblastoma and birth date: Evaluation of 3 U.S. datasets. Arch Environ Health. 59:26–30.
  • Hanchette CL, Schwartz GG. 1992. Geographic patterns of prostate cancer mortality. Evidence for a protective effect of ultraviolet radiation. Cancer. 70:2861–69.
  • Hannibal J, Fahrenkrug J. 2004. Melanopsin containing retinal ganglion cells are light responsive from birth. Neuroreport. 15:2317–20.
  • Harker JE. 1958. Experimental production of midgut tumours in periplaneta-Americana L. J Exp Biol. 35:251-&.
  • Heuch JM, Heuch I, Akslen LA, Kvale G. 1998. Risk of primary childhood brain tumors related to birth characteristics: A Norwegian prospective study. Int J Cancer. 77:498–503.
  • Higgins CD, Dos-Santos-Silva I, Stiller CA, Swerdlow AJ. 2001. Season of birth and diagnosis of children with leukaemia: An analysis of over 15 000 UK cases occurring from 1953-95. Br J Cancer. 84:406–12.
  • Hiroshige T, Honma K, Watanabe K. 1982. Prenatal onset and maternal modifications of the circadian rhythm of plasma corticosterone in blind infantile rats. J Physiol. 325:521–32.
  • Hoffman S, Schellinger KA, Propp JM, et al. 2007. Seasonal variation in incidence of pediatric medulloblastoma in the United States, 1995-2001. Neuroepidemiology. 29:89–95.
  • Horton TH. 1984. Growth and reproductive development of male Microtus montanus is affected by the prenatal photoperiod. Biol Reprod. 31:499–504.
  • Hu S, Ma F, Collado-Mesa F, Kirsner RS. 2004. Ultraviolet radiation and incidence of non-Hodgkin’s lymphoma among Hispanics in the United States. Cancer Epidemiol Biomarkers Prev. 13:59–64.
  • Huang PT, Spira AW, Wyse JP. 1983. Effects of alteration in the light cycle on outer segment shedding in the fetal retina. Invest Ophthalmol Vis Sci. 24:857–61.
  • Jackson CR, Capozzi M, Dai H, McMahon DG. 2014. Circadian perinatal photoperiod has enduring effects on retinal dopamine and visual function. J Neurosci. 34:4627–33.
  • Joechle W. 1964. Trends in Photophysiologic Concepts. Ann N Y Acad Sci. 117:88–104.
  • Johnson J, Wu V, Donovan M, et al. 2010. Melanopsin-dependent light avoidance in neonatal mice. Proc Natl Acad Sci U S A. 107:17374–78.
  • Kelleher FC, Rao A, Maguire A. 2014. Circadian molecular clocks and cancer. Cancer Lett. 342:9–18.
  • Koch HJ, Klinkhammer-Schalke M, Hofstadter F, et al. 2006. Seasonal patterns of birth in patients with glioblastoma. Chronobiol Int. 23:1047–52.
  • Kubatka P, Ahlersova E, Ahlers I, et al. 2002. Variability of mammary carcinogenesis induction in female Sprague-Dawley and Wistar: Hanrats: The effect of season and age. Physiol Res. 51:633–40.
  • Langagergaard V, Norgard B, Mellemkjaer L, et al. 2003. Seasonal variation in month of birth and diagnosis in children and adolescents with Hodgkin disease and non-Hodgkin lymphoma. J Pediatr Hematol Oncol. 25:534–38.
  • Lee TM, Spears N, Tuthill CR, Zucker I. 1989. Maternal melatonin treatment influences rates of neonatal development of meadow vole pups. Biol Reprod. 40:495–502.
  • Lewy AJ, Wehr TA, Goodwin FK, et al. 1980. Light suppresses melatonin secretion in humans. Science. 210:1267–69.
  • Lichtenstein P, Holm NV, Verkasalo PK, et al. 2000. Environmental and heritable factors in the causation of cancer--analyses of cohorts of twins from Sweden, Denmark, and Finland. N Engl J Med. 34:78–85.
  • Lin SW, Wheeler DC, Park Y, et al. 2012. Prospective study of ultraviolet radiation exposure and risk of cancer in the United States. Int J Cancer. 131:E1015–1023.
  • Lombardi C, Heck JE, Cockburn M, Ritz B. 2013. Solar UV radiation and cancer in young children. Cancer Epidemiol Biomarkers Prev. 22:1118–28.
  • Loscher W, Mevissen M, Haussler B. 1997. Seasonal influence on 7,12-dimethylbenz[a]anthracene-induced mammary carcinogenesis in Sprague-Dawley rats under controlled laboratory conditions. Pharmacol Toxicol. 81:265–70.
  • Lupi D, Sekaran S, Jones SL, et al. 2006. Light-evoked FOS induction within the suprachiasmatic nuclei (SCN) of melanopsin knockout (Opn4-/-) mice: A developmental study. Chronobiol Int. 23:167–79.
  • Mainio A, Hakko H, Koivukangas J, et al. 2006. Winter birth in association with a risk of brain tumor among a Finnish patient population. Neuroepidemiology. 27:57–60.
  • Makino K, Nakamura H, Hide T, et al. 2011. Risk of primary childhood brain tumors related to season of birth in Kumamoto Prefecture, Japan. Childs Nerv Syst. 27:75–78.
  • Mann DR, Akinbami MA, Gould KG, et al. 1993. Neonatal treatment of male monkeys with a gonadotropin-releasing hormone agonist alters differentiation of central nervous system centers that regulate sexual and skeletal development. J Clin Endocrinol Metab. 76:1319–24.
  • Manshande JP, Van Tornout J, Coppens M, Casaer P. 1985. Seasonal variation in incidence of cerebellar medulloblastoma. Brain Dev. 7:525–26.
  • Martynhak BJ, Correia D, Morais LH, et al. 2011. Neonatal exposure to constant light prevents anhedonia-like behavior induced by constant light exposure in adulthood. Behav Brain Res. 222:10–14.
  • McGrath JJ, Burne TH, Feron F, et al. 2010. Developmental vitamin D deficiency and risk of schizophrenia: A 10-year update. Schizophr Bull. 36:1073–78.
  • McMichael AJ, Giles GG. 1996. Have increases in solar ultraviolet exposure contributed to the rise in incidence of non-Hodgkin’s lymphoma? Br J Cancer. 73:945–50.
  • McNally RJ, Cairns DP, Eden OB, et al. 2002. An infectious aetiology for childhood brain tumours? Evidence from space-time clustering and seasonality analyses. Br J Cancer. 86:1070–77.
  • Meltzer AA, Annegers JF, Spitz MR. 1996. Month-of-birth and incidence of acute lymphoblastic leukemia in children. Leuk Lymphoma. 23:85–92.
  • Meltzer AA, Spitz MR, Johnson CC, Culbert SJ. 1989. Season-of-birth and acute leukemia of infancy. Chronobiol Int. 6:285–89.
  • Mendez N, Abarzua-Catalan L, Vilches N, et al. 2012. Timed maternal melatonin treatment reverses circadian disruption of the fetal adrenal clock imposed by exposure to constant light. Plos One. 7:e42713.
  • Mendez N, Halabi D, Spichiger C, et al. 2016. Gestational chronodisruption impairs circadian physiology in rat male offspring, increasing the risk of chronic disease. Endocrinology. 157:4654–68.
  • Mohr SB, Garland CF, Gorham ED, et al. 2011. Ultraviolet B and incidence rates of leukemia worldwide. Am J Prev Med. 41:68–74.
  • Morag I, Ohlsson A. 2013. Cycled light in the intensive care unit for preterm and low birth weight infants. Cochrane Database Syst Rev. 8:CD006982.
  • Nyari TA, Kajtar P, Bartyik K, et al. 2008. Seasonal variation of childhood acute lymphoblastic leukaemia is different between girls and boys. Pathol Oncol Res. 14:423–28.
  • Ohta H, Mitchell AC, McMahon DG. 2006. Constant light disrupts the developing mouse biological clock. Pediatr Res. 60:304–08.
  • Ono D, Honma S, Honma K. 2013. Postnatal constant light compensates Cryptochrome1 and 2 double deficiency for disruption of circadian behavioral rhythms in mice under constant dark. Plos One. 8:e80615.
  • Prendergast BJ, Gorman MR, Zucker I. 2000. Establishment and persistence of photoperiodic memory in hamsters. Proc Natl Acad Sci U S A. 97:5586–91.
  • Pyter LM, Nelson RJ. 2006. Enduring effects of photoperiod on affective behaviors in Siberian hamsters (Phodopus sungorus). Behav Neurosci. 120:125–34.
  • Rankin J, Silf KA, Pearce MS, et al. 2008. Congenital anomaly and childhood cancer: A population-based, record linkage study. Pediatr Blood Cancer. 51:608–12.
  • Reppert SM, Coleman RJ, Heath HW, Swedlow JR. 1984. Pineal N-acetyltransferase activity in 10-day-old rats: A paradigm for studying the developing circadian system. Endocrinology. 115:918–25.
  • Reppert SM, Schwartz WJ. 1983. Maternal coordination of the fetal biological clock in utero. Science. 220:969–71.
  • Reppert SM, Schwartz WJ. 1986a. Maternal endocrine extirpations do not abolish maternal coordination of the fetal circadian clock. Endocrinology. 119:1763–67.
  • Reppert SM, Schwartz WJ. 1986b. Maternal suprachiasmatic nuclei are necessary for maternal coordination of the developing circadian system. J Neurosci. 6:2724–29.
  • Roman E, Karlsson O. 2013. Increased anxiety-like behavior but no cognitive impairments in adult rats exposed to constant light conditions during perinatal development. Ups J Med Sci. 118:222–27.
  • Rosenwasser AM, Hayes MJ. 1994. Neonatal desipramine treatment alters free-running circadian drinking rhythms in rats. Psychopharmacology (Berl). 115:237–44.
  • Schmidt LS, Grell K, Frederiksen K, et al. 2009. Seasonality of birth in children with central nervous system tumours in Denmark, 1970-2003. Br J Cancer. 100:185–87.
  • Sekaran S, Lupi D, Jones SL, et al. 2005. Melanopsin-dependent photoreception provides earliest light detection in the mammalian retina. Curr Biol. 15:1099–107.
  • Selvin S, Levin LI, Merrill DW, Winkelstein W Jr. 1983. Selected epidemiologic observations of cell-specific leukemia mortality in the United States, 1969-1977. Am J Epidemiol. 117:140–52.
  • Simonneaux V. 2011. Naughty melatonin: How mothers tick off their fetus. Endocrinology. 152:1734–38.
  • Smith A, Lightfoot T, Simpson J, et al. 2009. Birth weight, sex and childhood cancer: A report from the United Kingdom childhood cancer study. Cancer Epidemiol. 33:363–67.
  • Sorensen HT, Pedersen L, Olsen J, Rothman K. 2001. Seasonal variation in month of birth and diagnosis of early childhood acute lymphoblastic leukemia. Jama. 285:168–69.
  • Sotak M, Sumova A, Pacha J. 2014. Cross-talk between the circadian clock and the cell cycle in cancer. Ann Med. 46:221–32.
  • Stiller CA, Parkin DM. 1990. International variations in the incidence of childhood lymphomas. Paediatr Perinat Epidemiol. 4:303–24.
  • Torres-Farfan C, Mendez N, Abarzua-Catalan L, et al. 2011. A circadian clock entrained by melatonin is ticking in the rat fetal adrenal. Endocrinology. 152:1891–900.
  • Tuthill CR, Freeman DA, Butler MP, et al. 2005. Perinatal influences of melatonin on testicular development and photoperiodic memory in Siberian hamsters. J Neuroendocrinol. 17:483–88.
  • Uchiwa T, Takai Y, Tashiro A, et al. 2016. Exposure of C57BL/6J mice to long photoperiod during early life stages increases body weight and alters plasma metabolomic profiles in adulthood. Physiol Rep. 4:18.
  • Van Laar M, Kinsey SE, Picton SV, Feltbower RG. 2013. First description of seasonality of birth and diagnosis amongst teenagers and young adults with cancer aged 15-24 years in England, 1996-2005. BMC Cancer. 13:365.
  • Van Leeuwen MT, Turner JJ, Falster MO, et al. 2013. Latitude gradients for lymphoid neoplasm subtypes in Australia support an association with ultraviolet radiation exposure. Int J Cancer. 133:944–51.
  • Van Steensel-Moll HA, Valkenburg HA, Vandenbroucke JP, Van Zanen GE. 1983. Time space distribution of childhood leukaemia in the Netherlands. J Epidemiol Community Health. 37:145–48.
  • Vanecek J, Illnerova H. 1982. Effect of photoperiod on the growth of reproductive organs and on pineal N-acetyltransferase rhythm in male rats treated neonatally with testosterone propionate. Biol Reprod. 27:517–22.
  • Varcoe TJ, Boden MJ, Voultsios A, et al. 2013. Characterisation of the maternal response to chronic phase shifts during gestation in the rat: Implications for fetal metabolic programming. Plos One. 8:e53800.
  • Varcoe TJ, Voultsios A, Gatford KL, Kennaway DJ. 2016. The impact of prenatal circadian rhythm disruption on pregnancy outcomes and long-term metabolic health of mice progeny. Chronobiol Int. 33:1171–81.
  • Varcoe TJ, Wight N, Voultsios A, et al. 2011. Chronic phase shifts of the photoperiod throughout pregnancy programs glucose intolerance and insulin resistance in the rat. Plos One. 6:e18504.
  • Vilches N, Spichiger C, Mendez N, et al. 2014. Gestational chronodisruption impairs hippocampal expression of NMDA receptor subunits Grin1b/Grin3a and spatial memory in the adult offspring. Plos One. 9:e91313.
  • Von Behren J, Reynolds P. 2003. Birth characteristics and brain cancers in young children. Int J Epidemiol. 32:248–56.
  • Wiesel TN, Hubel DH. 1963. Effects of visual deprivation on morphology and physiology of cells in the cats lateral geniculate body. J Neurophysiol. 26:978–93.
  • Yajima M, Matsumoto M, Harada M, et al. 2013. Effects of constant light during perinatal periods on the behavioral and neuronal development of mice with or without dietary lutein. Biomed Res. 34:197–204.
  • Yellon SM, Longo LD. 1988. Effect of maternal pinealectomy and reverse photoperiod on the circadian melatonin rhythm in the sheep and fetus during the last trimester of pregnancy. Biol Reprod. 39:1093–99.
  • Zuloaga DG, McGivern RF, Handa RJ. 2009. Organizational influence of the postnatal testosterone surge on the circadian rhythm of core body temperature of adult male rats. Brain Res. 1268:68–75.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.