Dynamic behavior of cell-free mitochondrial DNA in human saliva.


Journal

Psychoneuroendocrinology
ISSN: 1873-3360
Titre abrégé: Psychoneuroendocrinology
Pays: England
ID NLM: 7612148

Informations de publication

Date de publication:
09 2022
Historique:
received: 28 12 2021
revised: 20 05 2022
accepted: 23 06 2022
pubmed: 15 7 2022
medline: 4 8 2022
entrez: 14 7 2022
Statut: ppublish

Résumé

Mitochondria contain their own genome that can be released in multiple biofluids such as blood and cerebrospinal fluid, as cell-free mitochondrial DNA (cf-mtDNA). In clinical studies, blood cf-mtDNA predicts mortality and higher cf-mtDNA levels are associated with mental and physical stress. However, the dynamics of cf-mtDNA has not been defined, and whether it can be measured non-invasively like other neuroendocrine markers in saliva has not been examined. Here we report cf-mtDNA in human saliva and establish its natural within-person dynamic behavior across multiple weeks. In a small proof-of-principle cohort of healthy adults, we first develop an approach to rapidly quantify salivary cf-mtDNA without DNA isolation, and demonstrate the existence of salivary cf-mtDNA. We then deploy this approach to perform an intensive repeated-measures analysis of two healthy men studied at 4 daily timepoints over 53-60 consecutive days (n = 212-220 observations each) with parallel measures of steroid hormones, self-reported daily mood, and health-related behaviors. Salivary cf-mtDNA exhibited a robust awakening response reaching up to two orders of magnitude 30-45 min after awakening, varied from day-to-day, and moderately correlated with the cortisol awakening response. In exploratory analyses, no consistent association with self-reported daily mood/health-related behaviors were found, although this requires further examination in future studies. Dynamic variation in cf-mtDNA was inversely related with salivary interleukin 6 (IL-6), inconsistent with a pro-inflammatory effect of salivary cf-mtDNA. The highly dynamic behavior of salivary cf-mtDNA opens the door to non-invasive studies examining the relevance of mtDNA signaling in relation to human health.

Identifiants

pubmed: 35834882
pii: S0306-4530(22)00193-7
doi: 10.1016/j.psyneuen.2022.105852
pmc: PMC9880596
mid: NIHMS1864499
pii:
doi:

Substances chimiques

Cell-Free Nucleic Acids 0
DNA, Mitochondrial 0
Hydrocortisone WI4X0X7BPJ

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

105852

Subventions

Organisme : NIMH NIH HHS
ID : R01 MH119336
Pays : United States
Organisme : NIMH NIH HHS
ID : R01 MH122706
Pays : United States
Organisme : NIMH NIH HHS
ID : R21 MH123927
Pays : United States

Commentaires et corrections

Type : ErratumIn

Informations de copyright

Copyright © 2022 Elsevier Ltd. All rights reserved.

Références

Brain Behav Immun. 2013 Jan;27(1):38-41
pubmed: 22796263
Blood. 2014 Oct 2;124(14):2173-83
pubmed: 25082876
Clin Chem. 2004 Jan;50(1):213-6
pubmed: 14709653
FASEB J. 2020 Mar;34(3):3616-3630
pubmed: 31957088
Nat Med. 2012 Apr 15;18(5):759-65
pubmed: 22504485
PLoS Med. 2013 Dec;10(12):e1001577; discussion e1001577
pubmed: 24391478
Talanta. 2015 Oct 1;143:353-358
pubmed: 26078170
Mitochondrion. 2019 Sep;48:16-30
pubmed: 30771504
Neurosci Biobehav Rev. 2010 Sep;35(1):91-6
pubmed: 20109491
Transl Psychiatry. 2016 Dec 6;6(12):e971
pubmed: 27922635
Psychiatry Res. 1989 May;28(2):193-213
pubmed: 2748771
Nat Rev Endocrinol. 2014 May;10(5):303-10
pubmed: 24663223
Sleep. 2012 Jul 01;35(7):933-40
pubmed: 22754039
Proc Natl Acad Sci U S A. 2015 Dec 1;112(48):E6614-23
pubmed: 26627253
PLoS One. 2013 Jul 08;8(7):e68369
pubmed: 23861895
Psychoneuroendocrinology. 1994;19(4):313-33
pubmed: 8047637
Stem Cells. 2018 Sep;36(9):1404-1410
pubmed: 29781122
Eur J Immunol. 2014 May;44(5):1552-62
pubmed: 24470107
J Immunol. 1997 May 1;158(9):4454-64
pubmed: 9127011
J Dent Res. 2010 Oct;89(10):1016-23
pubmed: 20739693
Proc Natl Acad Sci U S A. 2010 Jun 15;107(24):10996-1001
pubmed: 20534480
Hum Genet. 2021 Apr;140(4):565-578
pubmed: 33123832
Biol Psychiatry. 2018 Jul 1;84(1):9-17
pubmed: 29525040
Cell Stress Chaperones. 2007 Winter;12(4):384-92
pubmed: 18229457
Mitochondrion. 2021 Jul;59:225-245
pubmed: 33839318
Sci Rep. 2018 May 2;8(1):6944
pubmed: 29720614
Proc Natl Acad Sci U S A. 2009 Mar 3;106(9):3543-8
pubmed: 19202080
Eur J Trauma Emerg Surg. 2018 Jun;44(3):325-334
pubmed: 29633007
Front Neuroendocrinol. 2018 Apr;49:72-85
pubmed: 29339091
Chronobiol Int. 2012 Aug;29(7):868-81
pubmed: 22823870
Front Immunol. 2019 Mar 19;10:502
pubmed: 30941136
Psychoneuroendocrinology. 2003 Jan;28(1):35-47
pubmed: 12445835
Biol Reprod. 2018 Jul 1;99(1):13-26
pubmed: 29718098
Proc Natl Acad Sci U S A. 2012 Sep 11;109(37):15036-41
pubmed: 22927403
Mitochondrion. 2009 Jul;9(4):261-5
pubmed: 19324101
Proc Natl Acad Sci U S A. 2006 Nov 7;103(45):17058-63
pubmed: 17075058
Nature. 2016 Jul 28;535(7613):561-5
pubmed: 27383793
Psychoneuroendocrinology. 2019 Sep;107:261-269
pubmed: 31174164
Nat Commun. 2015 Dec 09;6:8885
pubmed: 26648521
Blood. 2021 Jun 3;137(22):3116-3126
pubmed: 33661274
Neuropsychopharmacology. 2018 Jun;43(7):1557-1564
pubmed: 29453441
Proc Natl Acad Sci U S A. 2017 Oct 24;114(43):E9066-E9075
pubmed: 29073103
Assessment. 2002 Mar;9(1):41-55
pubmed: 11911234
Psychol Sci. 2007 Nov;18(11):991-8
pubmed: 17958714
Hypertension. 2000 Aug;36(2):303-7
pubmed: 10948094
Eur J Appl Physiol. 2015 Nov;115(11):2271-80
pubmed: 26126838
Biochim Biophys Acta. 2011 Oct;1813(10):1814-21
pubmed: 21664385
Transl Psychiatry. 2018 Oct 29;8(1):236
pubmed: 30374018
Mitochondrion. 2017 May;34:32-35
pubmed: 28017684
PLoS One. 2016 Nov 10;11(11):e0165799
pubmed: 27832117
Proc Natl Acad Sci U S A. 2012 Feb 14;109(7):2625-9
pubmed: 22308371
PLoS One. 2017 May 24;12(5):e0178216
pubmed: 28542490
Sci Rep. 2019 Mar 26;9(1):5220
pubmed: 30914716
Psychosom Med. 2004 Mar-Apr;66(2):207-14
pubmed: 15039505
Sci Rep. 2019 Dec 9;9(1):18607
pubmed: 31819080
Psychosom Med. 2018 Feb/Mar;80(2):141-153
pubmed: 29389736
Psychoneuroendocrinology. 2019 Aug;106:268-276
pubmed: 31029929
Proc Natl Acad Sci U S A. 2013 Aug 27;110(35):14468-73
pubmed: 23946426
Elife. 2021 Jun 15;10:
pubmed: 34128465
Physiol Rep. 2016 Jan;4(1):
pubmed: 26755735
Psychoneuroendocrinology. 2021 Sep;131:105336
pubmed: 34175558
Pers Soc Psychol Bull. 2007 Jan;33(1):69-84
pubmed: 17178931
J Pers Soc Psychol. 2003 Feb;84(2):365-76
pubmed: 12585810
Immunity. 2012 Aug 24;37(2):290-301
pubmed: 22863835
J Affect Disord. 2018 Jun;233:15-20
pubmed: 28633757
Front Endocrinol (Lausanne). 2016 Jul 29;7:106
pubmed: 27524977
Acta Psychiatr Scand. 2015 Sep;132(3):211-7
pubmed: 25891376
J Neurosci. 1997 Oct 15;17(20):7746-53
pubmed: 9315896
J Clin Endocrinol Metab. 2009 Mar;94(3):907-13
pubmed: 19088162
Psychoneuroendocrinology. 2016 Jan;63:414-32
pubmed: 26563991
Nature. 2010 Mar 4;464(7285):104-7
pubmed: 20203610
Clin Chem. 2020 Aug 1;66(8):1111-1114
pubmed: 32671378
Ageing Res Rev. 2019 Sep;54:100940
pubmed: 31415807

Auteurs

Caroline Trumpff (C)

Department of Psychiatry, Division of Behavioral Medicine, Columbia University Irving Medical Center, New York, USA.

Shannon Rausser (S)

Department of Psychiatry, Division of Behavioral Medicine, Columbia University Irving Medical Center, New York, USA.

Rachel Haahr (R)

Department of Psychiatry, Division of Behavioral Medicine, Columbia University Irving Medical Center, New York, USA.

Kalpita R Karan (KR)

Department of Psychiatry, Division of Behavioral Medicine, Columbia University Irving Medical Center, New York, USA.

Gilles Gouspillou (G)

Département des Sciences de l'Activité Physique, Faculté des Sciences, Université du Québec à Montréal (UQAM), Montreal, Québec, Canada.

Eli Puterman (E)

School of Kinesiology, University of British Columbia, Vancouver, Canada.

Clemens Kirschbaum (C)

Department of Psychology, TU Dresden, Germany.

Martin Picard (M)

Department of Psychiatry, Division of Behavioral Medicine, Columbia University Irving Medical Center, New York, USA; Department of Neurology, H. Houston Merritt Center, Columbia University Translational Neuroscience Initiative, Columbia University Irving Medical Center, New York, USA; New York State Psychiatric Institute, New York, USA. Electronic address: martin.picard@columbia.edu.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH