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Article ; Online: Fifty years on: How we uncovered the unique bioenergetics of brown adipose tissue.

Nicholls, David G

2023 Volume 237, Issue 4, Page(s) e13938

Abstract: Exactly 50 years ago, I was a post-doc in the laboratory of Olov Lindberg in Stockholm measuring fatty acid oxidation by mitochondria isolated from thermogenic brown adipose tissue, when we noticed a curious nonlinearity in the respiration rate. This ... ...

Abstract	Exactly 50 years ago, I was a post-doc in the laboratory of Olov Lindberg in Stockholm measuring fatty acid oxidation by mitochondria isolated from thermogenic brown adipose tissue, when we noticed a curious nonlinearity in the respiration rate. This initiated a convoluted chain of experiments revealing that the mitochondria were textbook demonstrations of the then novel and highly controversial "chemiosmotic hypothesis" of Peter Mitchell and that thermogenesis was regulated by a proton short-circuit, mediated by a 32 kDa "uncoupling protein," UCP1, activated by fatty acid. This review is a personal account of the research into the bioenergetics of isolated brown adipocytes and isolated mitochondria, which led, after fifteen years of investigation, to what is still accepted as the "canonical" UCP1-mediated mechanism of nonshivering thermogenesis, uniting whole animal physiology with mitochondrial bioenergetics.
MeSH term(s)	Animals ; Adipose Tissue, Brown/metabolism ; Mitochondrial Proteins/metabolism ; Mitochondria/metabolism ; Energy Metabolism ; Thermogenesis ; Fatty Acids/metabolism ; Uncoupling Protein 1/metabolism
Chemical Substances	Mitochondrial Proteins ; Fatty Acids ; Uncoupling Protein 1
Language	English
Publishing date	2023-02-06
Publishing country	England
Document type	Journal Article ; Review
ZDB-ID	2218636-0
ISSN	1748-1716 ; 1748-1708
ISSN (online)	1748-1716
ISSN	1748-1708
DOI	10.1111/apha.13938
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Article ; Online: Mitochondrial proton leaks and uncoupling proteins.

Nicholls, David G

Biochimica et biophysica acta. Bioenergetics

2021 Volume 1862, Issue 7, Page(s) 148428

Abstract: Non-shivering thermogenesis in brown adipose tissue is mediated by uncoupling protein 1 (UCP1), which provides a carefully regulated proton re-entry pathway across the mitochondrial inner membrane operating in parallel to the ATP synthase and allowing ... ...

Abstract	Non-shivering thermogenesis in brown adipose tissue is mediated by uncoupling protein 1 (UCP1), which provides a carefully regulated proton re-entry pathway across the mitochondrial inner membrane operating in parallel to the ATP synthase and allowing respiration, and hence thermogenesis, to be released from the constraints of respiratory control. In the 40 years since UCP1 was first described, an extensive, and frequently contradictory, literature has accumulated, focused on the acute physiological regulation of the protein by fatty acids, purine nucleotides and possible additional factors. The purpose of this review is to examine, in detail, the experimental evidence underlying these proposed mechanisms. Emphasis will be placed on the methodologies employed and their relation to the physiological constraints under which the protein functions in the intact cell. The nature of the endogenous, UCP1-independent, proton leak will also be discussed. Finally, the troubled history of the putative novel uncoupling proteins, UCP2 and UCP3, will be evaluated.
MeSH term(s)	Humans ; Membrane Potentials ; Mitochondria/metabolism ; Mitochondrial Proteins/metabolism ; Mitochondrial Uncoupling Proteins/metabolism ; Protons ; Thermogenesis
Chemical Substances	Mitochondrial Proteins ; Mitochondrial Uncoupling Proteins ; Protons
Language	English
Publishing date	2021-03-31
Publishing country	Netherlands
Document type	Journal Article ; Review
ZDB-ID	60-7
ISSN	1879-2650 ; 1879-2596 ; 1879-260X ; 1872-8006 ; 1879-2642 ; 1879-2618 ; 0006-3002 ; 0005-2728 ; 0005-2736 ; 0304-4165 ; 0167-4838 ; 1388-1981 ; 0167-4889 ; 0167-4781 ; 0304-419X ; 1570-9639 ; 0925-4439 ; 1874-9399
ISSN (online)	1879-2650 ; 1879-2596 ; 1879-260X ; 1872-8006 ; 1879-2642 ; 1879-2618
ISSN	0006-3002 ; 0005-2728 ; 0005-2736 ; 0304-4165 ; 0167-4838 ; 1388-1981 ; 0167-4889 ; 0167-4781 ; 0304-419X ; 1570-9639 ; 0925-4439 ; 1874-9399
DOI	10.1016/j.bbabio.2021.148428
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Article ; Online: A critical assessment of the role of creatine in brown adipose tissue thermogenesis.

Nicholls, David G / Brand, Martin D

Nature metabolism

2023 Volume 5, Issue 1, Page(s) 21–28

Abstract: Brown adipose tissue is specialized for non-shivering thermogenesis, combining lipolysis with an extremely active mitochondrial electron transport chain and a unique regulated uncoupling protein, UCP1, allowing unrestricted respiration. Current ... ...

Abstract	Brown adipose tissue is specialized for non-shivering thermogenesis, combining lipolysis with an extremely active mitochondrial electron transport chain and a unique regulated uncoupling protein, UCP1, allowing unrestricted respiration. Current excitement focuses on the presence of brown adipose tissue in humans and the possibility that it may contribute to diet-induced thermogenesis, countering obesity and obesity-related disease as well as protecting cardio-metabolic health. In common with other tissues displaying a high, variable respiration, the tissue possesses a creatine pool and mitochondrial and cytosolic creatine kinase isoforms. Genetic and pharmacological manipulation of these components have pleiotropic effects that appear to influence diet- and cold-induced metabolism in vivo and modeled in vitro. These findings have been used to advance the concept of a UCP1-independent diet-induced thermogenic mechanism based on a dissipative hydrolysis of phosphocreatine in beige and brown adipose tissue. Here we review the in vivo and in vitro experimental basis for this hypothesis, and explore alternative explanations. We conclude that there is currently no convincing evidence for a significant futile creatine cycle in these tissues.
MeSH term(s)	Humans ; Adipose Tissue, Brown/metabolism ; Creatine/metabolism ; Obesity/metabolism ; Diet ; Thermogenesis
Chemical Substances	Creatine (MU72812GK0)
Language	English
Publishing date	2023-01-09
Publishing country	Germany
Document type	Journal Article ; Review
ISSN	2522-5812
ISSN (online)	2522-5812
DOI	10.1038/s42255-022-00718-2
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Article: Mitochondrial proton leaks and uncoupling proteins

Nicholls, David G.

Biochimica et biophysica acta. 2021 July 01, v. 1862, no. 7

2021

Abstract	Non-shivering thermogenesis in brown adipose tissue is mediated by uncoupling protein 1 (UCP1), which provides a carefully regulated proton re-entry pathway across the mitochondrial inner membrane operating in parallel to the ATP synthase and allowing respiration, and hence thermogenesis, to be released from the constraints of respiratory control. In the 40 years since UCP1 was first described, an extensive, and frequently contradictory, literature has accumulated, focused on the acute physiological regulation of the protein by fatty acids, purine nucleotides and possible additional factors. The purpose of this review is to examine, in detail, the experimental evidence underlying these proposed mechanisms. Emphasis will be placed on the methodologies employed and their relation to the physiological constraints under which the protein functions in the intact cell. The nature of the endogenous, UCP1-independent, proton leak will also be discussed. Finally, the troubled history of the putative novel uncoupling proteins, UCP2 and UCP3, will be evaluated.
Keywords	H-transporting ATP synthase ; brown adipose tissue ; heat production ; mitochondria ; physiological regulation ; purine nucleotides
Language	English
Dates of publication	2021-0701
Publishing place	Elsevier B.V.
Document type	Article
ZDB-ID	282711-6
ISSN	0005-2728 ; 0304-4173
ISSN	0005-2728 ; 0304-4173
DOI	10.1016/j.bbabio.2021.148428
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Article ; Online: Fluorescence Measurement of Mitochondrial Membrane Potential Changes in Cultured Cells.

Nicholls, David G

Methods in molecular biology (Clifton, N.J.)

2018 Volume 1782, Page(s) 121–135

Abstract: The mitochondrial membrane potential is the dominant component of the proton-motive force that is the potential term in the proton circuit linking electron transport to ATP synthesis and other energy-dependent mitochondrial processes. Cationic ... ...

Abstract	The mitochondrial membrane potential is the dominant component of the proton-motive force that is the potential term in the proton circuit linking electron transport to ATP synthesis and other energy-dependent mitochondrial processes. Cationic fluorescent probes have been used for many years to detect gross qualitative changes in mitochondrial membrane potentials in intact cell culture. In this chapter I describe how these fluorescence signals may be used to obtain a semiquantitative measure of changes in mitochondrial membrane potential.
MeSH term(s)	Animals ; Cell Culture Techniques/instrumentation ; Cell Culture Techniques/methods ; Cells, Cultured ; Cerebellum/cytology ; Fluorescence ; Fluorescent Dyes/chemistry ; Membrane Potential, Mitochondrial ; Microscopy, Confocal/instrumentation ; Microscopy, Confocal/methods ; Microscopy, Fluorescence/instrumentation ; Microscopy, Fluorescence/methods ; Mitochondria/metabolism ; Neurons ; Rats ; Rhodamine 123/chemistry ; Rhodamines/chemistry ; Single-Cell Analysis/instrumentation ; Single-Cell Analysis/methods
Chemical Substances	Fluorescent Dyes ; Rhodamines ; tetramethylrhodamine methyl ester ; Rhodamine 123 (1N3CZ14C5O)
Language	English
Publishing date	2018-05-31
Publishing country	United States
Document type	Journal Article
ISSN	1940-6029
ISSN (online)	1940-6029
DOI	10.1007/978-1-4939-7831-1_7
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Article ; Online: Brain mitochondrial calcium transport: Origins of the set-point concept and its application to physiology and pathology.

Nicholls, David G

Neurochemistry international

2017 Volume 109, Page(s) 5–12

Abstract: The transport of calcium across the inner mitochondrial membrane plays a key role in neuronal physiology and pathology. The kinetic responses of the uniporter and efflux pathways are such that a cytosolic free calcium 'set-point' can be established - ... ...

Abstract	The transport of calcium across the inner mitochondrial membrane plays a key role in neuronal physiology and pathology. The kinetic responses of the uniporter and efflux pathways are such that a cytosolic free calcium 'set-point' can be established - above which there is net calcium accumulation into the matrix that is reversed when plasma membrane transport lowers cytosolic calcium. Pathological activation of N-methyl-d-aspartate receptor mediated sodium and calcium entry into the neuron, as occurs in stroke and spreading depression, places severe demands on both the ATP-generating and calcium loading capacities of the neuronal mitochondria as the set-point is exceeded. Experiments that led to the concept of the set-point are reviewed.
Language	English
Publishing date	2017-10
Publishing country	England
Document type	Journal Article ; Review
ZDB-ID	283190-9
ISSN	1872-9754 ; 0197-0186
ISSN (online)	1872-9754
ISSN	0197-0186
DOI	10.1016/j.neuint.2016.12.018
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Article ; Online: The hunt for the molecular mechanism of brown fat thermogenesis.

Nicholls, David G

Biochimie

2017 Volume 134, Page(s) 9–18

Abstract: This review focuses on research that my colleagues and I carried out from 1972 to 1986 that led to the identification of the original uncoupling protein and the development of the current model for the acute regulation of brown fat thermogenesis. An ... ...

Abstract	This review focuses on research that my colleagues and I carried out from 1972 to 1986 that led to the identification of the original uncoupling protein and the development of the current model for the acute regulation of brown fat thermogenesis. An important consequence of the early stages of this research was the realization that brown fat mitochondria demonstrated the key principles of Peter Mitchell's Chemiosmotic Hypothesis with exquisite precision and simplicity, that a regulatable proton conductance was necessary and sufficient to control respiration and hence thermogenesis, and that fatty acids provided not only the substrate for thermogenesis, but also acted as a self-regulating second (or third) messenger. These studies have provided the basis for 30 years of subsequent research by numerous groups into the structure and mechanism of UCP1, and its role in non-shivering thermogenesis in multiple species, including man.
MeSH term(s)	Adipocytes, Brown/cytology ; Adipocytes, Brown/metabolism ; Adipose Tissue, Brown/cytology ; Adipose Tissue, Brown/metabolism ; Animals ; Energy Metabolism/physiology ; Fatty Acids/metabolism ; Gene Expression Regulation ; Hibernation/physiology ; History, 20th Century ; History, 21st Century ; Humans ; Ion Transport ; Mitochondria/genetics ; Mitochondria/metabolism ; Mitochondrial Membranes/metabolism ; Proton-Motive Force ; Thermogenesis/physiology ; Uncoupling Protein 1/genetics ; Uncoupling Protein 1/history ; Uncoupling Protein 1/metabolism
Chemical Substances	Fatty Acids ; Uncoupling Protein 1
Language	English
Publishing date	2017-03
Publishing country	France
Document type	Historical Article ; Journal Article ; Review
ZDB-ID	120345-9
ISSN	1638-6183 ; 0300-9084
ISSN (online)	1638-6183
ISSN	0300-9084
DOI	10.1016/j.biochi.2016.09.003
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Article ; Online: The Pancreatic β-Cell: A Bioenergetic Perspective.

Nicholls, David G

Physiological reviews

2016 Volume 96, Issue 4, Page(s) 1385–1447

Abstract: The pancreatic β-cell secretes insulin in response to elevated plasma glucose. This review applies an external bioenergetic critique to the central processes of glucose-stimulated insulin secretion, including glycolytic and mitochondrial metabolism, the ... ...

Abstract	The pancreatic β-cell secretes insulin in response to elevated plasma glucose. This review applies an external bioenergetic critique to the central processes of glucose-stimulated insulin secretion, including glycolytic and mitochondrial metabolism, the cytosolic adenine nucleotide pool, and its interaction with plasma membrane ion channels. The control mechanisms responsible for the unique responsiveness of the cell to glucose availability are discussed from bioenergetic and metabolic control standpoints. The concept of coupling factor facilitation of secretion is critiqued, and an attempt is made to unravel the bioenergetic basis of the oscillatory mechanisms controlling secretion. The need to consider the physiological constraints operating in the intact cell is emphasized throughout. The aim is to provide a coherent pathway through an extensive, complex, and sometimes bewildering literature, particularly for those unfamiliar with the field.
MeSH term(s)	Animals ; Calcium/metabolism ; Energy Metabolism/physiology ; Glucose/metabolism ; Humans ; Insulin/metabolism ; Insulin-Secreting Cells/metabolism ; Ion Channels/metabolism ; Mitochondria/metabolism
Chemical Substances	Insulin ; Ion Channels ; Glucose (IY9XDZ35W2) ; Calcium (SY7Q814VUP)
Language	English
Publishing date	2016
Publishing country	United States
Document type	Journal Article ; Review
ZDB-ID	209902-0
ISSN	1522-1210 ; 0031-9333
ISSN (online)	1522-1210
ISSN	0031-9333
DOI	10.1152/physrev.00009.2016
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Article: Diagnostics and treatments of COVID-19: two-year update to a living systematic review of economic evaluations.

Elvidge, Jamie / Hopkin, Gareth / Narayanan, Nithin / Nicholls, David / Dawoud, Dalia

Frontiers in pharmacology

2023 Volume 14, Page(s) 1291164

Abstract: Objectives: ...

Abstract	Objectives:
Language	English
Publishing date	2023-11-16
Publishing country	Switzerland
Document type	Systematic Review
ZDB-ID	2587355-6
ISSN	1663-9812
ISSN	1663-9812
DOI	10.3389/fphar.2023.1291164
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Article: The hunt for the molecular mechanism of brown fat thermogenesis

Nicholls, David G

Biochimie. 2017 Mar., v. 134

2017

Abstract	This review focuses on research that my colleagues and I carried out from 1972 to 1986 that led to the identification of the original uncoupling protein and the development of the current model for the acute regulation of brown fat thermogenesis. An important consequence of the early stages of this research was the realization that brown fat mitochondria demonstrated the key principles of Peter Mitchell's Chemiosmotic Hypothesis with exquisite precision and simplicity, that a regulatable proton conductance was necessary and sufficient to control respiration and hence thermogenesis, and that fatty acids provided not only the substrate for thermogenesis, but also acted as a self-regulating second (or third) messenger. These studies have provided the basis for 30 years of subsequent research by numerous groups into the structure and mechanism of UCP1, and its role in non-shivering thermogenesis in multiple species, including man.
Keywords	brown adipose tissue ; fatty acids ; heat production ; mitochondria ; models ; proton-motive force
Language	English
Dates of publication	2017-03
Size	p. 9-18.
Publishing place	Elsevier B.V.
Document type	Article
ZDB-ID	120345-9
ISSN	0300-9084
ISSN	0300-9084
DOI	10.1016/j.biochi.2016.09.003
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