EAU 2021: Society of Urologic Oncology Lecture The VHL Kidney Cancer Gene: Discovery, Oxygen Sensing and Therapy

(UroToday.com) Dr. William Marston Linehan provides a lecture on the discovery, mechanism, and treatment paradigm for VHL kidney cancer as the invited Society of Urologic Oncology (SUO) lecturer at the European Association of Urology.


Dr. Linehan began this session with a talk focusing on the genetic basis of kidney cancer, including the implications for diagnosis and management. He emphasized that, while we initially thought of and treated all kidney tumors as the same, now we understand that kidney cancer represents a number of genetic and phenotypically diverse tumors all of which occur in the kidney.

 EAU 2021_genetic basis of kidney cancer,

 

Dr. Linehan emphasized that understanding the underlying biology helps us understand the appropriate treatment for each patient. In particular, in patients with localized disease, an understanding of the underlying biology can help guide us whether to observe or to intervene and, when intervening, how to do so. Similarly, in advanced disease, we may consider different systemic therapy approaches based on underlying tumor biology.

He began with their early experience with understanding the genetic basis of VHL at the National Cancer Institute (NCI). They began by focusing on patients with sporadic non-familial renal cell carcinoma. In 1987 (Zbar et al. Nature), they discovered that a loss of alleles on the short arm of chromosome 3 was associated with RCC – and thus began the VHL story. However, the human genome hadn’t yet been described so it wasn’t clear which genes may be involved.

He emphasized that most of what we now understand of the genetics of kidney cancer comes from studying inherited forms of kidney cancer. They shifted to family evaluations of kidney cancer to better understand the genetics and mechanisms of kidney cancer. While there are many genetically defined renal cell carcinoma syndromes, he emphasized four:

1. clear cell renal cell carcinoma: which may be either sporadic or associated with Von Hippel Lindau (VHL) disease.
2. type 1 papillary renal cell carcinoma: which, again, may be sporadic or associated with Hereditary Papillary Renal Carcinoma (HPRC)
3. type 2 papillary renal cell carcinoma: which may be sporadic or associated with Hereditary Leiomyomatosis Renal Cell Carcinoma (HLRCC)
4. Translocation RCC: which is also known as TFE3/TFEB RCC and may be associated with MITF.

While our understanding of these diseases has come from a study of patients with hereditary diseases, the conclusions are applicable to those with sporadic disease and have helped shape treatment for all patients with kidney cancer.

VHL disease, in addition to being characterized with renal tumors, is also associated with tumors of the adrenal gland, pancreas, brain or spine, eyes, and inner ears. Renal tumors tend to be bilateral, multifocal.

At the NCI, more than 1100 patients from more than 400 families with VHL have been evaluated and treated. This large exposure has helped to not just refine our understanding of the underlying biology, but also appropriate clinical decision making.

They have been aggressive with their surgical approach, initially with open approach and now with robotic approach. They routinely perform repeat partial nephrectomies (often for multiple tumors) to maximize surgical resection of these lesions.

Dr. Linehan emphasized that they have come to recommend active surveillance with a “3cm rule” where surgical intervention is recommended once the largest tumor reaches 3cm in maximal diameter. At the time of surgery, a nephron-sparing approach with tumor enucleation is advocated. He emphasized that, as of May 22, 2021, no patients with familial VHL have developed metastatic disease when managed this way. From a technical perspective, he highlighted that most patients are now managed with robotic-assisted partial nephrectomy with enucleation at level of pseudo capsule, sparing parenchyma.

He did note that the 3 cm rule doesn’t apply for all familial syndromes of RCC.

EAU 2021_familial syndromes of RCC 

 

Moving back to their work understanding the underlying pathogenesis of VHL-associated ccRCC, Dr. Linehan utilized linkage analysis leading to the identification of the VHL gene in the spring of 1993.

 EAU2021_underlying pathogenesis of VHL-associated ccRCC

Following identification of the VHL gene, and associated alterations in VHL-association ccRCC, they then wanted to know if the same gene was associated with sporadic ccRCC, finding that aberrations in VHL were found in more than 90% of patients with sporadic ccRCC.

Further work then sought to understand the function of the VHL gene. This understanding of the mechanism helps to guide the development of therapy for these patients.

VHL forms a complex to target HIF for ubiquitin-mediated degradation in an oxygen sensitive fashion: under normoxia, ubiquitination of HIF-α leads to its degradation. This fails in hypoxia and HIF-α accumulations. HIF is a transcription factor which drives transcription for VEGF, Glut-1, PDGF and others which contribute to a proliferative state.


EAU2021_HIF is a transcription factor 

In patients with VHL mutations, the VHL complex is unable to bind to HIF. As a result, in a parallel to hypoxic conditions, there is resulting HIF accumulation. Thus, VHL mutations create a pseudohypoxic condition. This work led to a Nobel prize for Dr. Kaelin, Ratcliffe, and Semenza in 2019.

Understanding these pathways has led to the development of 9 different targeted therapies. These target mTOR, the VEGF-receptor, the PDGFR-receptor, and the MET-receptor.

 EAU2021_VHL mutations_RCC

However, these agents act on targets that are important in other biologic functions, contributing to their toxicity. Thus, there is an ongoing interest to identify novel targets. Rather than addressing the downstream effects of HIF activation, they have focused on small molecular targeting of HIF-2α as a very selective treatment. Belzutifan (MK-6482) is a small molecule inhibitor of HIF-2α. Early trial data have suggested very good responses in patients with VHL disease. Presented at ASCO 2021 earlier this year, Srinivasan et al. noted an objective response rate of 49.1% in target RCC lesion, with responses shown below.

 

EAU_2021_Linehan_Choueiri_et_al_ASCO20.png 

Clinical trial data from Choueiri et al. (GU ASCO 20), demonstrated that 69% of patients had tumor shrinkage.


EAU_2021_Linehan_Choueiri_et_al_ASCO20_2.png

This was quite an expansive talk from the start of the VHL story to the current landscape of targeted therapy.



Presented by: William Marston Linehan, MD, Chief Urologic Oncology Branch, Senior Investigator, Center for Cancer Research
National Cancer Institute, Bethesda, MD

Written by: Thenappan (Thenu) Chandrasekar, MD – Urologic Oncologist, Assistant Professor of Urology, Sidney Kimmel Cancer Center, Thomas Jefferson University, @tchandra_uromd on Twitter during the 2021 European Association of Urology, EAU 2021- Virtual Meeting, July 8-12, 2021.