Activation of invasion by oncogenic reprogramming of cholesterol metabolism via increased NPC1 expression and macropinocytosis

Research output: Contribution to journalJournal articleResearchpeer-review

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Activation of invasion by oncogenic reprogramming of cholesterol metabolism via increased NPC1 expression and macropinocytosis. / Skorda, Aikaterini; Lauridsen, Anna Røssberg; Wu, Chengnan; Huang, Jinrong; Mrackova, Monika; Winther, Nuggi Ingholt; Jank, Vanessa; Sztupinszki, Zsofia; Strauss, Robert; Bilgin, Mesut; Maeda, Kenji; Liu, Bin; Luo, Yonglun; Jäättelä, Marja; Kallunki, Tuula.

In: Oncogene, Vol. 42, 2023, p. 2495–2506.

Research output: Contribution to journalJournal articleResearchpeer-review

Harvard

Skorda, A, Lauridsen, AR, Wu, C, Huang, J, Mrackova, M, Winther, NI, Jank, V, Sztupinszki, Z, Strauss, R, Bilgin, M, Maeda, K, Liu, B, Luo, Y, Jäättelä, M & Kallunki, T 2023, 'Activation of invasion by oncogenic reprogramming of cholesterol metabolism via increased NPC1 expression and macropinocytosis', Oncogene, vol. 42, pp. 2495–2506. https://doi.org/10.1038/s41388-023-02771-x

APA

Skorda, A., Lauridsen, A. R., Wu, C., Huang, J., Mrackova, M., Winther, N. I., Jank, V., Sztupinszki, Z., Strauss, R., Bilgin, M., Maeda, K., Liu, B., Luo, Y., Jäättelä, M., & Kallunki, T. (2023). Activation of invasion by oncogenic reprogramming of cholesterol metabolism via increased NPC1 expression and macropinocytosis. Oncogene, 42, 2495–2506. https://doi.org/10.1038/s41388-023-02771-x

Vancouver

Skorda A, Lauridsen AR, Wu C, Huang J, Mrackova M, Winther NI et al. Activation of invasion by oncogenic reprogramming of cholesterol metabolism via increased NPC1 expression and macropinocytosis. Oncogene. 2023;42:2495–2506. https://doi.org/10.1038/s41388-023-02771-x

Author

Skorda, Aikaterini ; Lauridsen, Anna Røssberg ; Wu, Chengnan ; Huang, Jinrong ; Mrackova, Monika ; Winther, Nuggi Ingholt ; Jank, Vanessa ; Sztupinszki, Zsofia ; Strauss, Robert ; Bilgin, Mesut ; Maeda, Kenji ; Liu, Bin ; Luo, Yonglun ; Jäättelä, Marja ; Kallunki, Tuula. / Activation of invasion by oncogenic reprogramming of cholesterol metabolism via increased NPC1 expression and macropinocytosis. In: Oncogene. 2023 ; Vol. 42. pp. 2495–2506.

Bibtex

@article{02df0218f4bf42f39a05b00a87cf6dc9,
title = "Activation of invasion by oncogenic reprogramming of cholesterol metabolism via increased NPC1 expression and macropinocytosis",
abstract = "Cancer cells are dependent on cholesterol, and they possess strictly controlled cholesterol homeostasis mechanisms. These allow them to smoothly switch between cholesterol synthesis and uptake to fulfill their needs and to adapt environmental changes. Here we describe a mechanism of how cancer cells employ oncogenic growth factor signaling to promote uptake and utilization of extracellular cholesterol via Myeloid Zinc Finger 1 (MZF1)-mediated Niemann Pick C1 (NPC1) expression and upregulated macropinocytosis. Expression of p95ErbB2, highly oncogenic, standard-treatment resistant form of ErbB2 mobilizes lysosomes and activates EGFR, invasion and macropinocytosis. This is connected to a metabolic shift from cholesterol synthesis to uptake due to macropinocytosis-enabled flow of extracellular cholesterol. NPC1 increase facilitates extracellular cholesterol uptake and is necessary for the invasion of ErbB2 expressing breast cancer spheroids and ovarian cancer organoids, indicating a regulatory role for NPC1 in the process. The ability to obtain cholesterol as a byproduct of increased macropinocytosis allows cancer cells to direct the resources needed for the energy-consuming cholesterol synthesis towards other activities such as invasion. These results demonstrate that macropinocytosis is not only an alternative energy source for cancer cells but also an efficient way to provide building material, such as cholesterol, for its macromolecules and membranes. [Figure not available: see fulltext.]",
author = "Aikaterini Skorda and Lauridsen, {Anna R{\o}ssberg} and Chengnan Wu and Jinrong Huang and Monika Mrackova and Winther, {Nuggi Ingholt} and Vanessa Jank and Zsofia Sztupinszki and Robert Strauss and Mesut Bilgin and Kenji Maeda and Bin Liu and Yonglun Luo and Marja J{\"a}{\"a}ttel{\"a} and Tuula Kallunki",
note = "Funding Information: This project has received funding from the Grosserer Alfred Nielsen og Hustrus Fond and from the European Union{\textquoteright}s Horizon 2020 Research and Innovation programme under grant agreement No 965193 for DECIDER (TK), from the Danish Cancer Society Scientific Committee (KBVU) R273-A16.084 (AS) and R228-A13637 (ZW), from the Danish National Research Foundation DNRF125 (MJ) and Novo Nordisk Foundation, NNF19OC0054296 (MJ). ",
year = "2023",
doi = "10.1038/s41388-023-02771-x",
language = "English",
volume = "42",
pages = "2495–2506",
journal = "Oncogene",
issn = "0950-9232",
publisher = "nature publishing group",

}

RIS

TY - JOUR

T1 - Activation of invasion by oncogenic reprogramming of cholesterol metabolism via increased NPC1 expression and macropinocytosis

AU - Skorda, Aikaterini

AU - Lauridsen, Anna Røssberg

AU - Wu, Chengnan

AU - Huang, Jinrong

AU - Mrackova, Monika

AU - Winther, Nuggi Ingholt

AU - Jank, Vanessa

AU - Sztupinszki, Zsofia

AU - Strauss, Robert

AU - Bilgin, Mesut

AU - Maeda, Kenji

AU - Liu, Bin

AU - Luo, Yonglun

AU - Jäättelä, Marja

AU - Kallunki, Tuula

N1 - Funding Information: This project has received funding from the Grosserer Alfred Nielsen og Hustrus Fond and from the European Union’s Horizon 2020 Research and Innovation programme under grant agreement No 965193 for DECIDER (TK), from the Danish Cancer Society Scientific Committee (KBVU) R273-A16.084 (AS) and R228-A13637 (ZW), from the Danish National Research Foundation DNRF125 (MJ) and Novo Nordisk Foundation, NNF19OC0054296 (MJ).

PY - 2023

Y1 - 2023

N2 - Cancer cells are dependent on cholesterol, and they possess strictly controlled cholesterol homeostasis mechanisms. These allow them to smoothly switch between cholesterol synthesis and uptake to fulfill their needs and to adapt environmental changes. Here we describe a mechanism of how cancer cells employ oncogenic growth factor signaling to promote uptake and utilization of extracellular cholesterol via Myeloid Zinc Finger 1 (MZF1)-mediated Niemann Pick C1 (NPC1) expression and upregulated macropinocytosis. Expression of p95ErbB2, highly oncogenic, standard-treatment resistant form of ErbB2 mobilizes lysosomes and activates EGFR, invasion and macropinocytosis. This is connected to a metabolic shift from cholesterol synthesis to uptake due to macropinocytosis-enabled flow of extracellular cholesterol. NPC1 increase facilitates extracellular cholesterol uptake and is necessary for the invasion of ErbB2 expressing breast cancer spheroids and ovarian cancer organoids, indicating a regulatory role for NPC1 in the process. The ability to obtain cholesterol as a byproduct of increased macropinocytosis allows cancer cells to direct the resources needed for the energy-consuming cholesterol synthesis towards other activities such as invasion. These results demonstrate that macropinocytosis is not only an alternative energy source for cancer cells but also an efficient way to provide building material, such as cholesterol, for its macromolecules and membranes. [Figure not available: see fulltext.]

AB - Cancer cells are dependent on cholesterol, and they possess strictly controlled cholesterol homeostasis mechanisms. These allow them to smoothly switch between cholesterol synthesis and uptake to fulfill their needs and to adapt environmental changes. Here we describe a mechanism of how cancer cells employ oncogenic growth factor signaling to promote uptake and utilization of extracellular cholesterol via Myeloid Zinc Finger 1 (MZF1)-mediated Niemann Pick C1 (NPC1) expression and upregulated macropinocytosis. Expression of p95ErbB2, highly oncogenic, standard-treatment resistant form of ErbB2 mobilizes lysosomes and activates EGFR, invasion and macropinocytosis. This is connected to a metabolic shift from cholesterol synthesis to uptake due to macropinocytosis-enabled flow of extracellular cholesterol. NPC1 increase facilitates extracellular cholesterol uptake and is necessary for the invasion of ErbB2 expressing breast cancer spheroids and ovarian cancer organoids, indicating a regulatory role for NPC1 in the process. The ability to obtain cholesterol as a byproduct of increased macropinocytosis allows cancer cells to direct the resources needed for the energy-consuming cholesterol synthesis towards other activities such as invasion. These results demonstrate that macropinocytosis is not only an alternative energy source for cancer cells but also an efficient way to provide building material, such as cholesterol, for its macromolecules and membranes. [Figure not available: see fulltext.]

U2 - 10.1038/s41388-023-02771-x

DO - 10.1038/s41388-023-02771-x

M3 - Journal article

C2 - 37420029

AN - SCOPUS:85164196472

VL - 42

SP - 2495

EP - 2506

JO - Oncogene

JF - Oncogene

SN - 0950-9232

ER -

ID: 360026542